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What is Environmental Robustness? Is it different from plasticity?

What is Environmental Robustness? Is it different from plasticity?



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Hansen (2006) in his review uses the concept ofenvironmental robustnessindependently of the other concepts of robustness (at pages 139 and 140) without defining it.

How is the termenvironmental robustnessusually defined?

The concept of robustness (aka genetic robustness) can be further decoupled into mutational robustness, developmental robustness and maybe some others. I think envirnmental robustness is one of these sub-categories of (genetic) robustness.

Intuitively, I understand environmental robustness as something that is very close toplasticity in the broad sense. What I callplasticity in the broad senseis any phenotypic response to an environment whether or not the response is adaptive or not. Therefore,plasticity in the broad senseisadaptive plasticity+non-adaptive plasticity. I would intuitively think that a genotype is environmentally robust if the phenotype it produces varies little with environment, that is if this genotype has low plasticity (in the broad sense). Am I using a more or less standard definition ofenvironmental robustness?


I think robustness and plasticity are different concepts, although related to each other.

I would define plasticity as the property of a system to adapt to external changes. As defined in the wikipedia page for phenotypic plasticity:

Phenotypic plasticity is the ability of an organism to change its phenotype in response to changes in the environment.

I think this definition agrees with the one in your question.

Robustness in biological systems, however, is defined as (wikipedia article):

Robustness of a biological system (also called biological or genetic robustness) is the persistence of a certain characteristic or trait in a system under perturbations or conditions of uncertainty.

From this article three references are cited, all of which give some definition of robustness in their introductions/abstracts:

Felix and Wagner (Heredity 2008):

Robustness, the persistence of an organismal trait under perturbations, is a ubiquitous property of complex living systems.

Kitano (Nature Reviews Genetics 2004):

Robustness is a property that allows a system to maintain its functions despite external and internal perturbations.

Stelling et al. (Cell 2004):

Robustness, the ability to maintain performance in the face of perturbations and uncertainty, is a long-recognized key property of living systems.

All these definitions imply that robustness is the ability to remain unperturbed under external or environmental perturbations. In a sense this looks like the opposite to plasticity, which is the ability to change under external perturbations. Personally, I think that robustness is accomplished because biological plasticity allows organisms to compensate (with some limits) the external perturbation in order to maintain their state.


I am just summarizing ddiez's answer with a small addition.

Robustness is the ability of the system to maintain its steady state or at the very least qualitative nature of the steady state with minor changes in the parameters of the system.

This is different from stability which actually means the ability of the system to return to its steady state when it is slightly displaced from there. A stable system will reach the steady state irrespective of the initial condition. In multistable systems the state where the system eventually converges, will depend on the initial condition.

So stability is meant in the sense of perturbation in the state and robustness, of perturbation in the system parameters.

So, if you have a model and you do a random sampling of parameters drawn from a uniform distribution of lets say ±2×mean, you will end up with a many sets of parameters with fluctuations from the mean values. Now, if you solve for the steady state at each parameter value you will get a distribution. Less the variance of this distribution, more robust is the system (based on the model).

We had discussed plasticity in this post. Plasticity may be in a way synonymous with adaptive; if a system takes an input and gives an output then how plastic a system is can be defined as how fast or easily does a system reach the new steady state. In this case the input is a parameter of the model and only that is changed.

If I put these concepts in the perspective of an organism's metabolism then:

  • Robustness would refer to how (in)sensitive the metabolic flux is to the minor changes in rates of different reactions (by changes in the enzyme structures perhaps).
  • Stability would refer to whether the system gets back (or how fast it gets back) to its original state if you add some extra or remove a metabolite.
  • Plasticity would refer to how fast would the system adapt or reach the new steady state when there is a change of diet/available nutrients.

Having said that I also feel, as fileunderwater said, that definitions are not universal and different people mean different things. Mathematically speaking environment is an extrinsic parameter i.e. Input. Environmental robustness should mean the maintenance of the steady state response to changes in the input. This makes sense for example in the case of maintenance of body temperature in homeotherms. Environmental plasticity is also important in certain situations.


How adaptive plasticity evolves when selected against

Adaptive plasticity allows organisms to cope with environmental change, thereby increasing the population’s long-term fitness. However, individual selection can only compare the fitness of individuals within each generation: if the environment changes more slowly than the generation time (i.e., a coarse-grained environment) a population will not experience selection for plasticity even if it is adaptive in the long-term. How does adaptive plasticity then evolve? One explanation is that, if competing alleles conferring different degrees of plasticity persist across multiple environments, natural selection between genetic lineages could select for adaptive plasticity (lineage selection). We show that adaptive plasticity can evolve even in the absence of such lineage selection. Instead, we propose that adaptive plasticity in coarse-grained environments evolves as a by-product of inefficient short-term natural selection: populations that rapidly evolve their phenotypes in response to selective pressures follow short-term optima, with the result that they have reduced long-term fitness across environments. Conversely, populations that accumulate limited genetic change within each environment evolve long-term adaptive plasticity even when plasticity incurs short-term costs. These results remain qualitatively similar regardless of whether we decrease the efficiency of natural selection by increasing the rate of environmental change or decreasing mutation rate, demonstrating that both factors act via the same mechanism. We demonstrate how this mechanism can be understood through the concept of learning rate. Our work shows how plastic responses that are costly in the short term, yet adaptive in the long term, can evolve as a by-product of inefficient short-term selection, without selection for plasticity at either the individual or lineage level.


What is Environmental Robustness? Is it different from plasticity? - Biology

PHENOTYPIC PLASTICITY AND NORMS OF REACTION

Phenotypic plasticity is the ability of individuals to alter its physiology, morphology and/or behavior in response to a change in the environmental conditions. This is clearly demonstrated by the appearance of plants grown at different densities: crowded plants look spindly and lanky, uncrowded plants look healthy and robust. In the context of evolution, phenotypic plasticity demonstrates the two meanings of adaptation: the plastic response is itself an example of a physiological adaptation and it is widely held that the ability to be plastic is adaptive in the sense of increasing fitness.

In thinking about phenotypic plasticity as a evolutionary adaptation it is important to separate the trait in question from the plasticity for that trait . For example: growing taller in response to plant crowding is adaptive in the sense that it increases an individual's competitive ability for sunlight (lower fitness when shaded by other plants). The "normal" height for a plant (lets assume there is such a thing) may have evolved in response to pressures to allocate resources to growth versus reproduction in a particular way. Thus there is a genetic basis for plasticity of plant height, and a genetic basis for plant height itself . The point is that different genes probably control these processes so the trait and its plasticity can (as opposed to must ) evolve independently.

Now consider the environment: certain physical properties of the environment can be described by the mean (average) value or the range of values (highest - lowest). Which aspect of an organism (the trait itself or the plasticity for that trait) will evolve in response to which measure? It may be that the plasticity for a trait will evolve in response to the range of values the environment throws at an organism (e.g., coldest - hottest, driest-wettest days), whereas the trait itself (e.g., thickness of fur) will evolve in response to the mean. This is not a rule! but would be an interesting thing to test and/or think about.

The idea of plasticity is interwoven with the notion of canalization . In light of the ball rolling down the trough of a developmental pathway (previous lecture), one can consider the width of the trough as an indication of the amount of plasticity "tolerated" in the organism in question. A highly canalized organism (or developmental program) would have low plasticity .

Another variant form of the plasticity issue is that some organisms may exhibit threshold effects where there is not a clear gradual transition between forms, but a stepwise change of phenotype in response to a gradual environmental change. See fig. 9.11, pg. 242, but note that these graphs do not have an environmental axis, so a distinct from a norm of reaction. One example of this are plants that have distinctly different growth forms in different environments. Question: is there an "environment" that is half way in between air and water?, and if so would these plants exhibit a graded response to such an environmental gradient?

A concept that places phenotypic plasticity in the context of a genotype-specific response is the norm of reaction . A norm of reaction is an array of phenotypes that will be developed by a genotype over an array of environments. The quantification of a norm of reaction is conceptually quite simple: one obtains a number of different genotypes (clonal pants are great for this) and grows each one in a variety of different environments (e.g., different nutrient, light, water conditions). After a period of growth one measures the desired trait(s) from each individual and plots the data out as shown in figure below this case for Drosophila bristles. Each line represents the data for a different genotype. If all lines are perfectly horizontal and on top of one another there is no effect of environment (E) or genotype (G) in case 1 below (each genotype is x, y or z). If all lines are not horizontal but on top of each other there is an environmental effect, but no genotype effect (case 2). If all lines are horizontal but at different positions there is no effect of environment but there is an effect of genotype (case 3 below). If lines not horizontal but are parallel there is an effect of environment and genotype, but there is no genotype x environment interaction (figure and case 4 below). If the lines are anything other than horizontal, there is an effect of environment. If the lines are neither horizontal nor parallel there is an effect of I) environment (nonhorizontality), ii) genotype (lines not on top of each other) and iii) genotype x environment interaction (not parallel case 5 below).

The interesting case comes when the norms of reaction lines cross. Then there is a range of environments where genotype 1 is "bigger" than genotype 2, where both genotypes are about the same and where genotype 2 is "bigger" than the genotype 1 (see figure below). Thus determining what is the "best" genotype, or the "fittest" genotype depends on the environment .


Developmental Plasticity: A Facilitator of Novelty

Environmental responsiveness and phenotypic plasticity are found everywhere in nature. All organisms are exposed to an environment and most of these environments are changing constantly, often in an unpredictable manner. Not surprisingly therefore, plasticity is found in all domains of life and at all levels of biological organization.

Developmental (phenotypic) plasticity describes the property of a genotype to respond to environmental variation by producing distinct phenotypes. The concept of plasticity dates back to the beginning of the 20th century and has continuously been developed to arrive at its current state, where many practitioners consider plasticity to represent a major facilitator of evolutionary diversification. In our lab, we investigate developmental plasticity at an integrative level.

HOW DO WE APPROACH PLASTICITY?

We are trying to answer the following questions:

1. What are the molecular mechanisms underlying developmental plasticity?
2. What is the evidence for plasticity as facilitator of novelty and what is it´s exact macro-evolutionary potential?
3. What are the evolutionary origins of plasticity?
4. How is environmental information becoming genetically encoded and integrated into the organism?

WHAT IS OUR MODEL SYSTEM?

We are using a mouth-form dimorphism in Pristionchus pacificus and its relatives to study the questions mentioned above.

P. pacificus and related nematodes lives on scarab beetles, i.e. cockchafers and stag beetles. Pristionchus waits for the beetle to die before exiting the arrested dauer stage. At that time, there is enormous competition for food and survival between many animals and microbes all living on the carcass.
It is long known that Pristionchus and relatives form teeth-like denticles in their mouth, which allow predatory feeding (see figure above). In the case of P. pacificus, animals decide during larval development in an irreversible manner to adopt a eurystomatous (Eu) or a stenostomatous (St) mouth-form. Eu animals form two teeth with a wide buccal cavity, representing predators. In contrast, St animals have a single tooth with a narrow buccal cavity and are strict microbial feeders. This dimorphism represents an example of phenotypic plasticity (Bento et al., 2010) and it is discrete and adaptive. Most importantly, mouth-form plasticity is regulated by conditional factors such as crowding, but also contains stochastic elements of regulation: a nearly constant ratio of 70-90% Eu : 30-10% St animals is formed under fixed environmental conditions. It is this aspect of stochastic regulation that allows manipulation of plasticity by genetic and molecular tools.

GENETIC AND EPIGENETIC REGULATION

Unbiased genetic screens resulted in the isolation of mutants that would only form one of the two mouth-forms and some of these mutants were characterized to represent “developmental switch genes”. eud-1 and nhr-40 mutants are monomorphic, being all-St and all-Eu, respectively (Ragsdale et al., 2013 Kieninger et al., 2016). Both genes are part of a developmental switch with loss-of-function and overexpression, resulting in complete, but opposite phenotypes. Developmental switches had long been predicted to play an important role in plasticity regulation, but due to the absence of genetic models of plasticity little genetic evidence was obtained. More recent studies in our lab began to investigate the epigenetic and potential trans-generational effects in the control of mouth-form plasticity.

MACRO-EVOLUTIONARY POTENTIAL OF PLASTICITY AND FACILITATION OF DIVERSITY

Is plasticity important for evolutionary diversification and novelty? Answering this question requires comparative studies that when performed in a phylogenetic context can provide insight into the significance of plasticity for evolutionary processes. Two recent studies have moved this analysis to the macro-evolutionary level, suggesting that phenotypic plasticity indeed facilitates rapid diversification. First, we studied the evolution of feeding structures in more than 90 nematode species using geometric morphometrics (Susoy et al., 2015). This study found that feeding dimorphism was indeed associated with a strong increase in complexity of mouth-form structures. At the same time, the subsequent assimilation of a single mouth-form phenotype coincided with a decrease in morphological complexity, but an increase in evolutionary rates.

A second case of mouth-form plasticity increasing morphological diversification came from a striking example of fig-associated Pristionchus nematodes (Susoy et al., 2016). These nematodes form five distinct mouth-forms that occur in succession in developing fig synconia, thereby increasing the polyphenism from two to five distinct morphs. Additionally, the morphological diversity of these five morphs exceeds that of several higher taxa, although all five morphs are formed by the same species. These findings strongly support the facilitator hypothesis and they also indicate that ecological diversity can be maintained in the absence of genetic variation as all this diversity is seen within a single species and without associated speciation and radiation events.

Scientists involved:

  • Mohannad Dardiry, Ph.D. Student
  • Dr. Catia Igreja, Staff Scientist
  • Dr. Ata Kalirad, Postdoc
  • Tess Renahan, Ph.D. Student
  • Devansh Sharma, Ph.D. Student
  • Shuai Sun, Ph.D. Student
  • Tobias Theska, Ph.D. Student
  • Sara Wighard, Ph.D. Student
  • Tobias Loschko, Technian (on leave)

Selected References:

Sieriebriennikov, B., Sun S., Lightfoot, J.W., Witte, H., Moreno, E., Rödelsperger, C., Sommer, R.J. (2020): Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell. PLOS Genetics. doi.org/10.1371/journal.pgen.1008687

Sommer, R.J. (2020): Phenotypic Plasticity: From Theory and Genetics to Current and Future Challenges. Genetics, Vol. 215, 1-13

Sieriebriennikov, B. & Sommer, R. J. (2018): Developmental plasticity and robustness of a nematode mouth-form polyphenism. Frontiers in Genetics. doi:10.3389/fgene.2018.00382

Namdeo, S., Moreno, E., Rödelsperger, C., Baskaran, P., Witte, H. & Ralf J. Sommer, R. J. (2018): Two independent sulfation processes regulate mouth-form plasticity in the nematode Pristionchus pacificus. Development, 145: dev166272.

Sieriebriennikov, B., Prabh, N., Dardiry, M., Witte, H., Rödelsperger, C., Röseler, W., Kieninger, M. R. & Sommer, R. J. (2018): A developmental switch generating phenotypic plasticity is part of a conserved multi-gene locus. Cell Reports, 23, 2835-2843.

Werner, M., Sieriebriennikov, B., Loschko, T., Namdeo, S., Lenuzzi, M., Renahan, T., Dardiry, M., Raj, D. & Sommer, R. J. (2017): Environmental influence on Pristionchus pacificus mouth-form through different culture methods. Scientific Reports, 7: 7207.

Serobyan, V. & Sommer, R. J. (2017): Developmental systems of plasticity and trans-generational inheritance in nematodes. Curr. Opin. Genet. & Devel., 45, 51-57.

Sieriebriennikov, B., Markov, G. V., Witte, H., & Sommer, R. J. (2017):The role of DAF-21/Hsp90 in mouth-form plasticity in Pristionchus pacificus. Molecular Biology & Evolution, 34, 1644-1653.

Serobyan, V., Xiao, H., Rödelsperger, C., Namdeo, S., Röseler, W., Witte, H. & Sommer, R. J. (2016):Chromatin remodeling and antisense-mediate up-regulation of the developmental switch gene eud-1 control predatory feeding plasticity. Nature Commun., 7: 12337.

Susoy, V., Herrmann, M., Kanzaki, N., Kruger, M., Nguyen, C.N., Rödelsperger, C., Röseler, W., Weiler, C., Giblin-Davis, R. M., Ragsdale, E. J. & Sommer, R. J. (2016): Large-scale diversification without genetic isolation in nematode symbionts of figs. Science Advance, 2: e1501031.

Susoy, V., Ragsdale, E. J., Kanzaki, N. & Sommer, R. J. (2015): Rapid diversification associated with a macroevolutionary pulse of developmental plasticity. eLIFE, 4: e05463.
Featured in: Nijhout, H.F. (2015): To plasticity and back again. eLIFE, 4: e06995.

Ragsdale, E. J., Mueller, M. R., Roedelsperger, C. & Sommer, R. J. (2013): A developmental switch coupled to the evolution of plasticity acts through a sulfatase. Cell, 155, 922-933.

Bento, G., Ogawa, A. & Sommer, R. J. (2010): Co-option of the hormone-signalling module dafachronic acid–DAF-12 in nematode evolution. Nature, 466, 494-497.


OMNAMO BIOLOGY CONCEPTS

PHENOTYPIC PLASTICITY AND NORMS OF REACTION

Phenotypic plasticity is the ability of individuals to alter its physiology, morphology and/or behavior in response to a change in the environmental conditions. This is clearly demonstrated by the appearance of plants grown at different densities: crowded plants look spindly and lanky, uncrowded plants look healthy and robust. In the context of evolution, phenotypic plasticity demonstrates the two meanings of adaptation: the plastic response is itself an example of a physiological adaptation and it is widely held that the ability to be plastic is adaptive in the sense of increasing fitness.
In thinking about phenotypic plasticity as a evolutionary adaptation it is important to separate the trait in question from the plasticity for that trait. For example: growing taller in response to plant crowding is adaptive in the sense that it increases an individual's competitive ability for sunlight (lower fitness when shaded by other plants). The "normal" height for a plant (lets assume there is such a thing) may have evolved in response to pressures to allocate resources to growth versus reproduction in a particular way. Thus there is a genetic basis for plasticity of plant height, and a genetic basis for plant height itself. The point is that different genesprobably control these processes so the trait and its plasticity can (as opposed to must) evolve independently.
Now consider the environment: certain physical properties of the environment can be described by the mean (average) value or the range of values (highest - lowest). Which aspect of an organism (the trait itself or the plasticity for that trait) will evolve in response to which measure? It may be that the plasticity for a trait will evolve in response to the range of values the environment throws at an organism (e.g., coldest - hottest, driest-wettest days), whereas the trait itself (e.g., thickness of fur) will evolve in response to the mean. This is not a rule! but would be an interesting thing to test and/or think about.
The idea of plasticity is interwoven with the notion of canalization. In light of the ball rolling down the trough of a developmental pathway (previous lecture), one can consider the width of the trough as an indication of the amount of plasticity "tolerated" in the organism in question. A highly canalized organism (or developmental program) would have low plasticity.
Another variant form of the plasticity issue is that some organisms may exhibit threshold effects where there is not a clear gradual transition between forms, but a stepwise change of phenotype in response to a gradual environmental change. See fig. 9.11, pg. 242, but note that these graphs do not have an environmental axis, so a distinct from a norm of reaction. One example of this are plants that have distinctly different growth forms in different environments. Question: is there an "environment" that is half way in between air and water?, and if so would these plants exhibit a graded response to such an environmental gradient?
A concept that places phenotypic plasticity in the context of a genotype-specific response is the norm of reaction. A norm of reaction is an array of phenotypes that will be developed by a genotype over an array of environments. The quantification of a norm of reaction is conceptually quite simple: one obtains a number of different genotypes (clonal pants are great for this) and grows each one in a variety of different environments (e.g., different nutrient, light, water conditions). After a period of growth one measures the desired trait(s) from each individual and plots the data out as shown in figure below this case for Drosophila bristles. Each line represents the data for a different genotype. If all lines are perfectly horizontal and on top of one another there is no effect of environment (E) or genotype (G) in case 1 below (each genotype is x, y or z). If all lines are not horizontal but on top of each other there is an environmental effect, but no genotype effect (case 2). If all lines are horizontal but at different positions there is no effect of environment but there is an effect of genotype (case 3 below). If lines not horizontal but are parallel there is an effect of environment and genotype, but there is no genotype x environment interaction (figure and case 4 below). If the lines are anything other than horizontal, there is an effect of environment. If the lines are neither horizontal nor parallel there is an effect of I) environment (nonhorizontality), ii) genotype (lines not on top of each other) and iii) genotype x environment interaction (not parallel case 5 below).


The interesting case comes when the norms of reaction lines cross. Then there is a range of environments where genotype 1 is "bigger" than genotype 2, where both genotypes are about the same and where genotype 2 is "bigger" than the genotype 1 (see figure below). Thus determining what is the "best" genotype, or the "fittest" genotype depends on the environment.


S2 (issue 6)- Plasticity & DNA Methylation: When, Where and How?

I have been fascinated with the question of how organisms can adapt to the environment for a long time and in particular the genetic basis behind such adaptation. This adaptation can take place partly through micro- evolutionary changes i.e. changes in the allele frequency of a population over time, but another important mechanism is also phenotypic plasticity: the within-individual change in phenotype in response to different environments. It is clear that phenotypic plasticity is a very important mechanism by which organisms respond and thus adapt to the environment. It is also clear that plasticity can have a genetic basis.

One trait that I’ve been particularly interested in is the seasonal timing of reproduction, i.e. when in the year an organism reproduce. Variation in timing of reproduction is important because individuals need to match when they reproduce with the peak in food resources in order to optimize fitness, if you breed much too early or much too late there will be very little food around (mismatched) and so there is strong selection on timing of reproduction.

Organisms receive several different cues from the environment about when they should initiate reproduction and these include for example photoperiod, temperature as well as different social cues. But how is information from these environmental cues incorporated into the body to start initiating breeding and what genetic mechanism might control this?

Regulatory genes play a big role here and thus mechanisms that control gene regulation, such as DNA methylation, are involved in the control of seasonal reproduction in species such as Siberian hamsters, the plant Arabidopsis and also in other species. It is now possible to measure DNA methylation at a genome wide level also in non-model organisms using bisulfite treatment of DNA before sequencing and thus obtain nucleotide level resolution of methylation levels. However, it is well known that RNA expression as well as methylation patterns can be highly tissue specific. Yet we often sample blood on vertebrates when assessing methylation because we do not necessarily have access to the particular tissue (at least not without sacrificing the individual) we know is involved in sensing the environmental cue. But how well do methylation patterns we see in blood reflect methylation patterns in the tissues that are involved in sensing of the environmental cues? And, more specifically when looking at timing of reproduction: are changes in DNA methylation in the tissue of relevance reflected in the blood?

This is what I have reviewed in my article. The answer? Well, it is certainly possible to find examples of studies that demonstrate a correlation between (changes in) DNA methylation across tissues. This suggest that DNA methylation measured in blood can be informative of methylation changes taking place in other tissues. However, the robustness and generality of this is still unclear. Hopefully more studies will soon allow us to provide a more accurate answer to this very important question as the answer will be an integral part of the experimental design of future epigenetic studies in natural populations.

Arild Husby is an assistant professor at Uppsala University interested in the genetic basis of complex traits and the evolutionary forces operating on them using natural populations of birds and insects as model systems. With a background in quantitative genetics (PhD from Edinburgh University in 2010) he has increasingly focused on trying to identify regions of the genome that control complex traits and the evolutionary forces operating on them. Research in his lab currently focuses on epigenetic regulation of timing of reproduction using birds as model and the regulatory changes involved in wing polyphenism using water striders as a model. You can find more about his research here: https://www.ieg.uu.se/evolutionary-biology/husby-lab/husby-research/

read the upcoming issue 6 with s2 included by Dec 15th via https://academic.oup.com/icb

Husby’s paper:

“On the use of blood samples for measuring DNA methylation in ecological epigenetic studies”


The role of developmental plasticity in evolutionary innovation

Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.

1. Introduction

Identifying the factors that promote the origin of complex, novel traits is among the most intriguing and enduring problems in evolutionary biology [1]. It is intriguing because it lies at the heart of what motivates much of evolutionary biology: to understand the origins of exquisite adaptations, and the transitions and radiations that they fuelled. It is enduring because it embodies a fundamental paradox. On the one hand, Darwin's theory of evolution is based on descent with modification, wherein everything new, ultimately, must come from something old [2]. On the other hand, biologists are captivated by complex novel traits precisely because they often lack obvious homology to pre-existing traits [3]. How, then, does novelty arise within the confines of ancestral developmental patterns and variation?

In this review, we describe how the study of developmental plasticity can offer significant insights into the origins of evolutionary innovation. We define evolutionary innovation broadly, ranging from the expression of traits or trait variants that are themselves novel to the expression of existing traits in new behavioural, physiological or morphological contexts. Developmental plasticity, in turn, is defined as a single genotype's ability to alter its developmental processes and phenotypic outcomes in response to different environmental conditions. Such environmental effects on trait expression can range from modest adjustments to growth rate or tissue allocation in response to resource levels, to dramatic polyphenic switches by which a single genotype can give rise to discrete and often radically different alternative phenotypes [4]. Intriguingly, many innovations of macroevolutionary significance also occur as facultatively expressed alternatives in related lineages (figure 1 electronic supplementary material, table S1). This raises the central questions our article aims to address: can major novel traits originate as plastic, environment-dependent alternatives to already established, ancestral phenotypes? If so, what are the mechanisms by which developmental plasticity may mediate the initiation and subsequent elaboration of incipient novel traits?

Figure 1. Environmentally dependent polyphenism in various taxa. (a) The water flea Daphnia longicephala develops protective crests and tail spines in response to its water bug predator, Notonecta. Differences in coat colour and texture are produced in Arctic fox (Vulpes lagopus) in response to seasonal change. (b) When a bluehead wrasse (Thalassoma bifasciatum) male (blue morph) is removed from his harem, a female (yellow morph) will change phenotype completely and become a male. The gaudy commodore, Precis octavis, is seasonally dimorphic. In the wet season, it has an orange wing and in the dry season the wings are bluish purple in colour. Onthophagus nigriventris dung beetles metamorphose as horned major males or hornless sneaker males in response to ample or insufficient larval feeding resources, respectively. (c) The tiger salamander (Ambystoma tigrinum) only metamorphoses if its aquatic environment becomes uninhabitable. Larval nutrition determines major and minor worker development in Pheidole rhea. The morphology of white water-buttercup (Ranunculus aquatilis) leaves depends on their environment. Submerged leaves are branched into 20 or more thread-like segments. Floating or exposed leaves are scalloped.

The notion that plasticity promotes innovation is not new. Indeed, researchers have suggested for over a century that developmental plasticity is crucial in the formation of evolutionary novelties (reviewed in [5]). What is new, however, is that we are finally beginning to grasp the underlying mechanisms by which developmental plasticity might promote innovation. Our goal is therefore to integrate knowledge of these mechanisms with theory and thereby explain how developmental plasticity promotes innovation. We begin by reviewing the causes, mechanisms and consequences of genetic accommodation, a process by which environmentally induced phenotypes can become subject to heritable modification [5–7]. We then explore the means by which developmental and genetic mechanisms associated with environmentally induced alternatives influence the subsequent evolutionary potential of a lineage. Finally, we investigate the developmental genetic architectures that underlie environment-dependent trait expression and discuss their implications for the evolutionary origin of novel traits.

2. Genetic accommodation and innovation

Genetic accommodation is adaptive genetic change owing to selection on the regulation and form of a mutationally or environmentally induced novel phenotype [5,8,9]. Genetic accommodation does not require new mutations to occur, but it might incorporate such mutations along with standing genetic variation, including variants that were formerly cryptic, neutral or rare in a population. Genetic accommodation improves the function and integration of novel traits, and diminishes harmful pleiotropic effects. Genetic accommodation can also promote the persistence of developmental plasticity, refine the conditions under which alternative traits are expressed and enhance the precision of environmental matching. In extreme cases, such as when a population is exposed to a novel but relatively invariant environment, the novel phenotype can become constitutive, a phenomenon referred to as genetic assimilation [10]. Below, we briefly discuss the properties of development that fuel evolution by genetic accommodation. We then highlight empirical studies that advance our understanding of the significance of evolution by genetic accommodation.

(a) Developmental and genetic mechanisms underlying genetic accommodation

Organisms have evolved a diverse array of homeostatic mechanisms to buffer or canalize development against environmental perturbations. These mechanisms are best understood in metabolic and physiological systems, but are also beginning to be elucidated in developmental genetic systems. Such mechanisms include feedback regulation, duplicate or redundant pathways, a balance between antagonistic processes and switch-like behaviour [11,12]. Several partially redundant homeostatic mechanisms may be at work simultaneously in a given system, a redundancy that further stabilizes the phenotype. Importantly, these same mechanisms can also protect a developing organism from genetic perturbations owing to mutations [13,14] (but see [15]). By acting as a phenotypic buffer against both environmental and genetic perturbations, homeostatic mechanisms permit the accumulation of greater genetic variability than would be possible in their absence. Cryptic genetic variation that accumulates in this manner is a component of, rather than separate from, the standing genetic variation in a population. Specifically, it represents standing variation that is phenotypically unexpressed under certain environmental or genetic circumstances and, as such, contributes to the potential for either genotype-by-environment or epistatic interactions to influence the evolutionary process.

The expression and rapid evolution of novel phenotypes become possible when the phenotypic effects of accumulated genetic variation become expressed though a change in the environment or a sensitizing mutation. Once expressed, such formerly cryptic genetic variation does not differ fundamentally from standing genetic variation for constitutively expressed traits. However, being unexpressed under a subset of conditions allows cryptic genetic variation that is neutral or even deleterious in some environments to persist in a population, analogous to models for recessive alleles.

How then does evolution by genetic accommodation differ from adaptive evolution as traditionally understood? In many ways, evolution by genetic accommodation provides a shift in emphasis, rather than a radically new view of adaptive evolution. Traditional neo-Darwinian perspectives on adaptive evolution generally envision a ‘waiting for a mutation’ process [16], by which adaptations emerge from the gradual accumulation and fixation of mutations that change phenotype expression in a direction favoured by selection. In such models, standing genetic variation is usually presented in the context of an equilibrium between new mutations and removal by selection (mutation–selection balance). Environmental conditions are important, because they determine the nature and direction of selection, whereas development provides the means by which genotype is translated into phenotype.

Although both genetic variation and the selective role of the environment remain key factors, evolution by genetic accommodation differs from this traditional model in two critical ways. First, it ascribes the additional role to the environment of releasing novel phenotypes that express previously accumulated genetic variation. In other words, the environment plays a formative as well as a selective role. Environmental perturbations can operate immediately on the level of populations and may persist for generations, potentially releasing substantial heritable variation to confront new conditions. Second, evolution by genetic accommodation emphasizes the role of developmental processes in determining which genetic variants will be manifested in selectable, phenotypic differences and under what environmental circumstances this will occur [5]. Critically, environment-dependent development permits genetic variants to be neutral under a larger set of circumstances, and thus to be hidden from selection, and allowed to drift and accumulate in natural populations. Evolution by genetic accommodation therefore expands beyond a traditional neo-Darwinian model by recognizing that the interplay between environment and development provides a mechanism for both the accumulation and the rapid release of genetic variation in the face of novel environmental challenges.

But what evidence exists to suggest that genetic accommodation can indeed yield novel, adaptive phenotypes under new conditions, and that this process shapes the evolutionary trajectories of natural populations?

(b) Artificial selection experiments demonstrate genetic accommodation

The earliest demonstration of evolution by genetic accommodation through artificial selection was Waddington's study on cross-vein expression on Drosophila [17]. Cross veins contribute to torsional stiffness of the wing, and vary in presence/absence and position within the Diptera [18]. When exposed to ecologically relevant temperature stress during development, flies expressed phenotypic variation for loss of cross veins, otherwise observed at low frequency in natural populations (0.5%). Using artificial selection, Waddington demonstrated that this variation was heritable, and that the initially induced phenotype could rapidly become constitutively expressed in a population. Waddington and others further demonstrated that a variety of phenotypes could become genetically assimilated under artificial selection [19]. Subsequent work demonstrated that unexpressed standing genetic variation was responsible [20], and that segregating variation was widespread in natural populations [21]. Similar results for plants were obtained by Huether [22,23], who demonstrated that the rare expression of flower morph variants in Linanthus was, in part, the result of environmental stress experienced by plants in the field. Huether then demonstrated that such stress-induced variation was indeed heritable via artificial selection, suggesting that here, too, environmental conditions were responsible for revealing selectable heritable variation.

More recently, laboratory studies on a broad array of organisms (including Drosophila [15,24], Arabidopsis [25], fungi [26] and Lepidoptera [8]) have focused on the role of temperature stress and heat shock proteins as a means of releasing selectable phenotypic diversity (but see [27]). In these studies, environmental stress resulted in a remarkable increase in the amount of selectable phenotypic variation, mediating rapid responses to artificial selection—including some reminiscent of naturally evolved phenotypes [8]. Artificial selection experiments have thus demonstrated unequivocally that developmental systems confronted with challenging environments can expose novel phenotypic variants, which in turn provide sufficient substrate for rapid, selective evolution of novel forms.

(c) Genetic accommodation in natural populations

Demonstrating that genetic accommodation has occurred in natural populations is considerably more challenging than demonstrating that it can occur in the laboratory. If genetic accommodation has played a role in the evolution of a particular novel trait, then we would predict that patterns of plasticity in ancestral populations should resemble the constitutively expressed trait differences observed in derived populations. A major impediment to testing this prediction is that ancestral populations are usually no longer available for study, making it difficult to characterize ancestral reaction norms. The best systems for testing this prediction are therefore those in which ancestral populations are extant [28–30]. Below, we describe several studies in which genetic accommodation has been inferred in natural populations.

Our first example comes from the house finch (Carpodacus mexicanus). Carpodacus mexicanus has colonized a remarkable range of environments during its recent invasion of North America, with resulting populations exhibiting extensive differentiation in physiological responses to environmental variation, including the induction of incubating behaviour and associated hormones in response to temperature variation. Available data indicate that such responses have been fine-tuned from plastic ancestors to produce local adaptation, giving rise to populations with divergent reproductive attributes after only 14 generations [29]. Systems that have undergone such recent and rapid evolution (see also [31]) provide excellent opportunities to accurately describe ancestral patterns of developmental plasticity.

Comparisons of longer-separated populations allow us to determine whether ancestral plasticity can contribute to greater novelty than that observed during contemporary evolution. An example comes from the most recent diversification of three-spine stickleback fish initiated as glaciers retreated 12 000 years ago. As oceanic stickleback invaded shallow lakes, giving rise to bottom-feeding (benthic) populations, and deep lakes, giving rise to planktivorous (limnetic) populations, differences in habitat use favoured differentiation of suites of functionally integrated traits including trophic morphology, body form and behaviour. Experiments reveal that ancestral, oceanic populations exhibit phenotypic plasticity that parallels differentiation among independently replicated freshwater benthic and limnetic ecotypes, but which are of lesser magnitude [32,33]. These results are consistent with the possibility that ancestral plasticity has guided the evolution of more extreme features characteristic of the derivative ecotypes. Combined, these examples demonstrate how ancestral plasticity can be refined or enhanced in derived populations.

When a single aspect of the phenotype is strongly favoured, canalization of an initially inducible response can also evolve rapidly. For example, introduction of salmonid predators to alpine lakes inhabited by the zooplankter Daphnia melanica has led to a loss of plasticity in an antipredator defence [34]. Melanin protects D. melanica from UV light but renders them conspicuous to piscine predators. Following the introduction of salmonid predators to two lakes, D. melanica exhibited a substantial decline in UV-mediated plasticity of melanin production relative to that expressed in predator-free populations. Where predators were introduced, Daphnia exhibited constitutive upregulation of the arthropod melanin gene ebony and Ddc (dopa decarboxylase), both responsible for the adaptive reduction of melanin production. Reduced plasticity has also evolved in populations of three-spine stickleback from geologically recent (post-glacial) freshwater lakes in the expression of sodium–potassium ATPase (ATP1A1) [35] with adaptation to fresh water, and in New World spadefoot toad species that exhibit constitutively short larval development as a result of their short natal pond durations [36]. Additional evidence of genetic assimilation is found in the apparent loss of ancestral polyphenisms across diverse taxa (electronic supplementary material, table S1).

Two important insights arise from the preceding examples. First, comparisons of ‘ancestral’ and derived populations may vary with respect to how long such populations have diverged, presenting a potential trade-off between the accuracy of assessing ancestral reaction norms, and the uniqueness of a novel, derived trait. Secondly, although these examples demonstrate patterns consistent with those we would expect from genetic accommodation [5,10], the fundamental features of this process—that environmental stimuli initiate genetic and selection processes—make it impossible to discriminate cases of natural selection on environmentally dependent versus constitutively expressed variation once natural selection has occurred [37]. Nevertheless, the evidence for an environmentally dependent origin of novelty is, in such cases, as strong as that for an origin based on constitutively expressed standing genetic variation.

3. Developmental plasticity and evolvability

Developmental plasticity can increase the evolutionary potential, or ‘evolvability’, of developmental systems in three important ways, thereby increasing a lineage's potential for diversification and innovation. We discuss each of these three ways separately below.

(a) Developmental plasticity provides new targets for evolutionary processes

Once environmentally mediated development has evolved, the underlying mechanisms can promote evolutionary diversification by increasing the points in ontogeny at which change can potentially arise, thus increasing the degrees of evolutionary freedom [38]. A consensus is emerging that diversity in multicellular organisms primarily reflects changes in the regulatory interactions that shape gene expression [39–41]. Highly complex regulatory interactions are precisely what characterize plastic phenotypic expression [42]. In plastic developmental systems, environmental conditions influence development at various points in ontogeny via multiple external and somatic signals. External signals are transduced into cellular ones by means of hormones, metabolites, receptor molecules, nervous signals, osmotic changes and physical interactions among cells. This broad and diverse regulatory dimensionality dramatically increases the potential evolutionary change points. Additionally, because these regulatory systems are highly epistatic, change in any one genetic element can lead to novel phenotypic effects [38].

Furthermore, the different components underlying plastic regulatory systems can evolve independently of one another, thereby diversifying the evolutionary trajectories available to a lineage, including those that may eventually lead to novel, adaptive phenotypes. Such diverse evolutionary opportunities are exemplified by the many cases of threshold evolution in insects [4,19,43], evolved divergences in response cues and response mechanisms in plants [44,45], and timing and magnitude of plastic responses in amphibians [46,47].

(b) Plasticity promotes novelty by providing ‘re-usable’ building blocks for development

Plastic developmental systems also promote evolutionary novelty because shared regulatory modules—including both the transduction or switch mechanism and the downstream pathways of phenotypic expression—can be re-used and recombined in new ways in different descendent taxa and environmental circumstances. Several recent studies reveal how a common transduction event can activate divergent phenotypic responses. In plants, for instance, phytochromes are a family of photo-convertible molecules found in above-ground plant cells that initiate the complex signalling pathways involved in shade plasticity [48]. Phytochromes are activated by specific wavelengths of transmitted and reflected light that stimulate sensitive and rapid growth adjustments, such as stem and petiole elongation that lifts leaves away from shade cast by neighbouring plants—a ‘shade-avoidance syndrome’ shown to be adaptive [49]. Interestingly, plants have evolved to use the phytochrome sensory system to switch on an entirely different suite of plastic responses: the production of defensive compounds in response to herbivory via the jasmonate signalling pathway [50]. Both shade avoidance and defence plasticity use this diffuse sensory system, which can read environmental conditions at any of the plant's leaves or branches to initiate either elongation or biosynthetic responses within minutes. Similarly, in insects, the same endocrine machinery plays a critical role in coordinating alternative reproductive decisions (whether to invest in growth and maintenance or reproduction), alternative developmental decisions (moulting and metamorphosis) and polyphenic development (facultative diapause, host switch, caste and morph expression [51]). Re-use and recombination of developmental machinery underlying plastic responses have also been implicated in nematode evolution, where dafachronic acid (DAF-12)-mediated induction of dauer-stage formation (an adaptive response to food shortage widespread across nematodes) has become co-opted to mediate the induction of alternative feeding morphologies in at least one species, Pristionchus pacificus [52].

Conversely, different environmental cues and transduction events can make use of a shared hormonal pathway or other common downstream module, ‘re-using’ that response pathway to produce a similar plastic outcome in a novel ecological situation [42]. For instance, the plastic ‘shade avoidance’ response mentioned above consists largely of stem and petiole elongation. Rapid elongation of these same structures is also an essential plastic response to a plant's submergence under water (which can occur episodically in wetland habitats [53]). Both shade and flooding elongation responses are governed by shared hormonal pathways that interact with the DELLA family of growth-restraining proteins and expansin genes that affect cell-wall extensibility [48,54,55]. Yet these shared developmental pathways are initiated by entirely different environmental switches: light spectral composition in the case of shade avoidance and submergence-induced build-up of the gaseous hormone ethylene in case of flooding elongation [55].

(c) Developmental plasticity creates novel trait interactions

Patterns of phenotypic correlation among developmentally or functionally related traits vary from one environment to another when some or all of the constituent traits express plasticity [56,57]. As a result, plastic developmental systems can give rise to new trait interactions, trait covariances and fitness trade-offs that contribute to evolutionary diversification, as reported for learning ability in cabbage white butterflies [58] and diet-induced horn expression in beetles [59]. However, plasticity does not always result in a trade-off between traits: environmentally induced morphologies may simply act as a platform for the modification of additional traits that work well as a suite. For example, a shrimp diet can produce a short-gut morphology in species of spadefoot toads that do not normally consume shrimp. In other species, however, this environmentally induced change in gut morphology is accompanied by a suite of functionally integrated traits that jointly comprise a distinct ecological response [60]. The phylogenetic relationships of these lineages suggest that diet-induced gut plasticity in spadefoots was followed by the evolution of these drastic modifications of behavioural, morphological and physiological plasticity. Plastic traits that differ among related species can also interact with constitutive species-specific traits to shape environment-specific fitness outcomes [56].

These examples illustrate that, just as plasticity can contribute novel targets for evolutionary change, it may also help generate novel trait interactions. Accordingly, developmental plasticity may cause species and populations to diverge in many more traits than those specifically targeted by a given evolutionary mechanism. Such trait interactions can pose pleiotropic constraints on adaptive evolution, but also have the potential to shift the evolutionary trajectories available to lineages into phenotypic and ecological space that otherwise would remain unexplored.

4. Developmental genetic basis of plastic traits: mechanisms and consequences

The developmental genetic basis of conditional traits is just beginning to be explored, yet it is already clear that diverse mechanisms underlie environment-dependent trait expression [61]. Here, we briefly examine the implications of two extremes in a continuum of developmental control architectures. At one end of this continuum, the same developmental genetic network can mediate the expression of alternative phenotypes across environments by altering the nature of interactions between network components through environment-specific regulatory elements. For example, comparative gene expression data suggest that winged and wingless ant castes are produced developmentally through caste-specific interruption of the same wing-patterning network [62]. Although the points of interruption may differ among different wingless castes of the same species (as well as between species), the same network is involved in each case. Similarly, in horned beetles the same developmental mechanism—programmed cell death—is involved in generating both sexual and alternative male dimorphisms in horn expression [63], and recent microarray studies show that sexes and morphs overlap substantially in patterns of gene expression [64]. In such pleiotropic systems, the independent evolution of alternative phenotypes can be constrained, as evolutionary changes affecting expression of one phenotype will affect other phenotypes regulated by the same developmental genetic network. These constraints would be relaxed only during periods when a given alternative morph was rare or absent.

At the same time, shared mechanisms can maintain a developmental system's ability to express environment-specific traits even during prolonged periods of environmental stasis when certain alternatives are not elicited. In this case, re-expression of such traits in descendent lineages, or their co-option into novel contexts, may become feasible with only minor evolutionary changes in the underlying developmental genetic network. Indeed, loss and recurrence of complex traits has been demonstrated in a number of cases [65], and co-option of ancestral developmental networks during the genesis of novel complex traits appears to be a ubiquitous feature of developmental evolution [66]. However, it remains unclear whether developmental plasticity and polyphenic development enhance retention and co-option of developmental pathways, or whether both emerge simply as a product of the integrated nature of development in general.

At the other end of the mechanistic continuum, distinct genes and gene networks may mediate the expression of alternative environmentally contingent phenotypes. Context-specific gene expression is extremely widespread [67] and may have evolved under selection to supersede the pleiotropic constraints discussed above, permitting organisms to fine-tune gene expression in each environmental context. Additionally, environment-specific gene expression can have unique and fundamentally important evolutionary consequences not shared by other types of context-specific expression. While tissue- and stage-specific expression occurs in every individual in a population, environment-specific expression is restricted to those individuals within a population and generation that encounter a given environment. If selective environments are coarse-grained (i.e. each individual encounters only one environment during its lifetime), then environmental frequencies determine the proportion of individuals within a population that expresses a given set of environment-specific phenotypes and underlying gene networks. Genes for which expression is restricted to a subset of individuals in each generation are predicted to experience relaxed selection, because mutations occurring in gene copies that reside in individuals who do not express these genes are hidden from selection. Mutations thus accumulate faster in these genes than they do in genes that are expressed in every individual [68].

Relaxed selection on components of environment-specific gene-regulatory networks provides a population-genetic mechanism by which developmental plasticity can contribute to the evolution of new traits. Specifically, population-genetic models predict that (i) the extent of mutation accumulation should scale with the proportion of unexpressed gene copies in a population [69] (ii) conditionally expressed genes may diverge many times faster between species than similar genes for which expression is condition-insensitive [70] and (iii) during prolonged periods of environmental stasis, genes that are not expressed may undergo rapid degradation and loss of function owing to continued mutation accumulation [67]. (iv) Additionally, periods of environmental stasis (and consistent selection) should allow genes that have become constitutively expressed to undergo rapid bursts of adaptive evolution, enabled, in part, by mutations accumulated during prior periods of relaxed selection on those genes.

The first three of these predictions are supported by a growing body of empirical evidence (reviewed in [67]). For instance, bacterial quorum-sensing genes, induced only when certain population densities are reached, show increased levels of variation within species when compared with similar, constitutively expressed genes [68]. In horn-polyphenic beetles, genes that are more specific to alternative morphs show greater divergence than genes for which expression is shared across morphs [64] and in aphids, where sexual and asexual generations alternate, such that males are often expressed only once every 10–20 female generations, male-specific genes exhibit greatly accelerated divergence more consistent with relaxed selection than positive selection [71]. Studies on microbes also provide substantial support for the third prediction (i.e. that unexpressed genes should rapidly accumulate mutations and degrade during periods of environmental stasis [72]).

But what about the converse? As we propose above, genes that become constitutively expressed during periods of stasis should be subject to the full strength of positive selection rather than relaxed selection, such that mutations and mutation combinations accumulated during prior periods of relaxed selection on such genes can now promote their rapid adaptive evolution. Although little direct evidence is presently available to test this hypothesis, numerous studies have highlighted the importance of cryptic genetic variation that can be released during shifts into novel or stressful environments [73,74] to facilitate rapid adaptive evolution through genetic accommodation. Relaxed selection on environment-specific genes may provide a key mechanism by which such variations may accumulate.

We have discussed shared versus alternative developmental genetic networks as extremes along a continuum of models for the regulation of plastic trait expression. In real organisms, both types of regulatory architecture are probably involved, depending on the organism, trait and level of biological organization in question. Indeed, gene-expression surveys provide ample evidence that both environment-shared and environment-specific expression patterns are widespread [67]. Moreover, both types of regulation can apply to the same trait at different levels of a developmental genetic network: upstream regulators such as transcription factors tend to be highly pleiotropic, whereas their downstream targets may be expressed in a highly context-specific manner, and thus more likely to become subject to relaxed selection. Both regulatory models can even apply simultaneously to different parts of the same gene: protein-coding regions may be transcribed across environments, while the action of promoters may be environment-specific. A similar situation may apply in cases of context-specific splicing of exons (e.g. [75]).

Clearly, further integration of molecular, developmental and evolutionary mechanisms of conditional trait expression will require a much more detailed understanding of the developmental genetic machinery that underlies plasticity. Here, traditional as well as emerging model systems in developmental and evolutionary genetics have the potential to make important, cross-fertilizing contributions. For instance, the role of dafachronic acid signalling has been studied in detail in the regulation of dauer-stage formation in the nematode and genetic model system Caenorhabditis elegans, and recent work has begun to explore the developmental co-option of the same pathway in the regulation of derived alternative feeding morphologies in related genera [52]. Similarly, a combination of population genetic and mapping studies on pea aphids permitted the identification of the aphicarus locus (which influences both sex- and environment-specific wing expression [76]), the regulatory role for which is currently being studied using candidate genes and pathways identified primarily through studies on Drosophila wing development [77]. Finally, the increasing availability and affordability of genetic and genomic techniques permit their application directly onto organisms famous for their developmental plasticity, such as water fleas [78] or honeybees [79].

5. Conclusions and future directions

Developmental plasticity has long been posited to play a key role in the origin and diversification of novel traits. With recent theoretical and technical advances, it is now possible to critically test this broad hypothesis in the laboratory and field. However, a number of key questions are as yet unanswered. Below, we highlight five specific questions that provide fruitful avenues for future research into plasticity's role in innovation.

First, do most novel traits indeed begin as conditionally expressed alternative phenotypes? Recent theoretical considerations [5] suggest that novel, complex traits probably start out as alternative phenotypes within populations. However, more empirical studies are needed to assess the generality of plasticity's role in the origins of novelty. An effective approach is to assess patterns of ancestral plasticity in lineages that have given rise to taxa expressing derived novelties to evaluate whether ancestral plasticity might have provided the raw material for these novel traits. A broad range of such studies will also reveal whether these transitions are more often moderate and quantitative or macroevolutionary in nature.

Second, how is developmental plasticity stabilized to produce novel phenotypes? Genetic accommodation occurs when evolutionary processes act on quantitative genetic variation underlying environmentally dependent traits, thereby enhancing or diminishing plasticity. However, we know very little about the developmental and genetic mechanisms enabling plastic responses to be stabilized as novel traits.

Third, what is the nature of genetic variation that fuels evolution by genetic accommodation? Studies are needed to determine the degree to which evolution by genetic accommodation is fuelled by: (i) constitutively versus conditionally expressed genetic variation (ii) novel mutations versus standing genetic variation (iii) rare versus common allelic variants (iv) differential expression of the same gene networks versus separate regulatory gene networks (v) changes in upstream regulator genes versus downstream target genes (vi) changes in promoter versus coding regions (vii) changes in cis-regulation or trans-regulatory factors and (viii) few or many genes of either large or small effect.

Fourth, how common is genetic accommodation in natural populations? Although genetic accommodation has been demonstrated in the laboratory [8], the frequency and importance of genetic accommodation in nature is unclear. Studies in the wild are especially relevant, given that many natural environments are undergoing dramatic and rapid changes owing to global climate change, habitat degradation and the increased presence of invasive species. At the same time, genetic and genomic screening techniques, from bar-coding to next-generation sequencing, are now available well outside molecular model systems. Such methods would permit population-wide changes in phenotypic variation to be correlated with genome- or transcriptome-wide surveys of variation patterns at DNA and transcript levels, as populations encounter, respond and adapt to profound environmental changes.

Finally, can we develop models that realistically integrate developmental plasticity into a population genetics framework? As evolutionary biologists use qualitative and quantitative models to explore the role of environmental trait induction and its influence on the direction and rate of evolution, future research needs to test the assumptions and predictions of these models. For instance, most current models make implicit and explicit simplifying assumptions about the developmental genetic architecture underlying plastic traits, about how environments can influence trait expression, and about the co-variation between the roles of environment as inductive and selective agents. Empirical verification of these assumptions will allow for a robust theoretical framework to be developed to complement and motivate empirical studies.


5 CONCLUSIONS

Our results support the growing evidence of a link between functional similarity and niche similarity, as well as between trait hierarchies and differences in competitive ability (i.e. fitness differences). Both were related to invasion dynamics of non-native ornamentals, but their effect depended on the vital rate analysed and on the drought stress level experienced by the community. Overall, we showed that community resistance to potential ornamental invasions is shaped by both niche-based and hierarchical competition mechanisms. Functionally distinct ornamental herbs, which are taller and have smaller and denser leaves geared to conserve water, are likely to better tolerate biotic resistance of central European native grassland communities and therefore might have a better chance to succeed in the invasion process. However, our findings suggest that the level of environmental stress, in particular drought stress, can affect the intensity and mode of biotic resistance in these native communities, potentially reducing its strength towards growth and reproduction of escaped ornamental species. Trade-offs and demographic compensation processes may also lead to greater invasiveness (i.e. expansion due to fast growth and reproduction) of ornamental plants in native communities. Finally, we showed that ignoring plastic responses to competition might lead to overlooking an important mechanism by which those ornamental species which are already most competitive tolerate biotic resistance, making them even more worrisome. Even though our results are based on a selection of European grassland species under relatively artificial conditions in mesocosms, functional differences, environmental stress, vital rates and competition-induced trait plasticity are likely to play an important role for biotic resistance across other types of native communities. Future experimental and field studies aimed at unravelling the mechanisms of biotic resistance to the next generation of plant invaders across habitats should not neglect the plastic response of non-native species to competition as well as changing competitive outcomes under different stress levels.


Genes shyness

In the December 2005 issue of Psychological Science, researchers at the University of Maryland found that children with a particular variant of the serotonin transporter gene whose mothers reported low social support were more likely to be shy. However, if their mothers had plenty of social support, children with this variant were at no greater risk of shyness. The protein produced by the short form of the gene is known to predispose toward some forms of stress sensitivity (such as anxiety). In followup work published in the February 2007 issue of Current Directions in Psychological Science, the team found that mothers of naturally shy children may respond to their children in less nurturing fashion, reinforcing the children’s fearfulness and shyness.

Sources: Fox NA, Nichols KE, Henderson HA, Rubin K, Schmidt L, Hamer D, et al. 2005. Evidence for a gene𠄾nvironment interaction in predicting behavioral inhibition in middle childhood. Psychol Sci 16(12):921�.

Fox NA, Hane AA, Pine DS. 2007. Plasticity for affective neurocircuitry: how the environment affects gene expression. Curr Dir Psychol Sci 16(1):1𠄵.


What is Environmental Robustness? Is it different from plasticity? - Biology

Coping with climate change
May 2009

2009 is the Year of Science! This year-long party celebrates all of science. Find out what's happening in your neighborhood at www.yearofscience2009.org.

Many recent changes in organisms have been chalked up to climate change. Which of those represent adaptation and which represent phenotypic plasticity? Here are a few examples from each category:

    Canadian squirrels have evolved earlier breeding times. Squirrels with genes for earlier breeding were probably favored because this allows them to take advantage of an earlier spring and hoard more pinecones for winter survival.

    Some plant species around Walden Pond are flowering as much as three weeks earlier than they did 150 years ago. In these species, flowering is partly triggered by temperature, so climate change is the likely cause of this shift.

Evolutionary biology has a special term to describe changes in an individual organism over the course of its lifetime: phenotypic plasticity. That's a mouthful, but the idea is straightforward. An organism's phenotype is simply its set of features, and to be plastic means to be moldable or changeable — so phenotypic plasticity just means that an organism's features can be molded, or influenced to some degree, by its environment. You can think of it as the "nurture" side of the nature/nurture debate. The concept encompasses all sorts of changes to individual organisms, including developmental changes (e.g., an organism reaching a larger body size if it gets good nutrition as a juvenile, but reaching a smaller size on poor nutrition), behavioral changes (e.g., a polar bear eating goose eggs instead of seals, if seals become hard to catch and eggs are plentiful), and physical changes (e.g., a rabbit that grows white fur in the winter and brown fur in the summer). Phenotypic plasticity includes any sort of change to an individual that isn't caused by changes in its genes.

Telling the difference between evolutionary adaptation and phenotypic plasticity can be tricky because, like adaptations, changes due to plasticity often make a lot of sense in terms of an organism's survival and reproduction. After all, a polar bear that eats goose eggs when nothing else is available, will probably up its chances of survival. Changes due to phenotypic plasticity are often advantageous for the organism because plasticity itself can evolve by natural selection. The idea here is that, while eating goose eggs is not itself an evolutionary adaptation, the ability to switch to different food sources when the need arises is an adaptation and was favored over the bears' evolutionary history. A rabbit's white winter fur is not itself an adaptation, but the physical mechanisms for changing fur colors with the seasons are adaptations. And while putting on a t-shirt is not an adaptation, having the smarts to recognize that it's hot out and to figure out what to do about it is an important human adaptation. How phenotypically plastic a species is (and in what ways) can evolve over time.

When you hear references in the media to organisms "adapting" to climate change, it's worth considering what is really meant by this. Are the organisms actually evolving, or are they experiencing changes in behavior or physical traits that can be chalked up to phenotypic plasticity? The difference is important. For one thing, some changes due to plasticity are intentional. We humans will adjust to a warming planet by changing how we live because we are actively trying to make these modifications. Other changes due to plasticity are not intentional at all. A plant species that winds up growing further and further north as the Earth warms is not "trying" to adjust its range. This range shift is the result of environmental and physiological factors that the plant doesn't control. Most importantly, actual evolutionary adaptations are never intentional. For example, scientists have discovered that, as the climate has warmed in recent decades, Canadian squirrels have evolved shifts in their breeding times that make them more successful in warmer climates. This shift was caused, not by environmental factors, but by changes in the genetic make-up of the population — and so, represents true evolutionary adaptation. The squirrels did not acquire these genetic changes by "trying" or deciding to breed at different times. Their evolution was the simple result of genetic variation and an environment that favored some gene versions (gene versions that affected the timing of breeding) over others. When the term adapt is used to describe all these different sorts of changes — some evolutionary, some not, some intentional, some not — it's easy to get confused about the mechanism of change being discussed.


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