Evolvability has emerged as the connection between population-level evolution and macroevolution. Although both of these processes are fundamentally the same (both occurring through mutation, drift, and selection), they happen at such different scales that we typically use very different tools and mindsets to study each of them. For example, population-level evolution is often modeled with Hardy-Weinberg related equations examining the fitness and prevalence of particular alleles. On the other hand, we typically study macroevolutionary change by comparing distinct species using the fossil record and molecular genetics. The question is, then, how do we go from here to there? How do these micro-level processes eventually result in macro-level patterns? Evolvability is one useful way to approach this. A population is "evolvable" if it can cope with changing environments via adaptation. That is, genetic mutations in the population have a good chance of increasing fitness.
While at the surface level, this seems simplistic, we can follow it to deeper levels to see how the evolvability of a population affects developmental processes whose evolution underlies macroevolutionary changes. Gerhart and Kirschner tackle this in their paper the Theory of Facilitated Variation. In this paper they identify major routes by which developmental genetic changes can "facilitate" (or help increase) phenotypic variation without compromising fitness (i.e. they increase evolvability).
These routes, termed weak regulatory linkage, exploratory processes, and compartmentation, are summarized below:
Ability to engage in weak regulatory linkage
Linkage occurs between processes that are connected to each other or to specific conditions. For example, when you are cold you shiver and get goosebumps. These two processes are connected to each other via a condition (cold) and also via the sympathetic nervous system. Likewise, developmental processes can be linked via shared gene regulatory networks and/or via shared regulatory components (for example genes that are expressed in response to the same transcription factor, or signal transduction pathways that respond to the same signaling molecule).
Weak regulatory linkage refers to linked processes that are regulated by simple inputs that do not provide much information to the processes. We have seen examples of this in Habits of Highly Effective Signalling Pathways, where a transcription factor releases repression on a set of downstream genes. These genes self-activate via local activators as soon as the inhibition is released suggesting there could potentially be multiple ways to de-inhibit them. This is considered weak regulatory linkage because the regulation by the transcription factor is "weak." When local activators are present, the default for the process is "on". The transcription factor is only needed to release inhibition. Once this inhibition is released, a cascade of gene expression can occur, resulting in a complex process with large developmental or physiological consequences. In this way a complex process can be turned off or turned on in new places with small-scale regulatory changes. For example, the transcription factor expression can be turned up or down, or other proteins can act to modify the ability of the transcription factor to bind to its target DNA.
In general, weak regulatory linkage occurs when a simple signal can trigger multiple complex processes depending on the cellular context. Gerhart and Kirschner note that this increases the plasticity of a system since small changes to the regulatory factors (transcription factors for example) can change the functional output of a complex system. The complex system itself is largely self-regulating, requiring only a trigger from the regulatory factors. In this way, development can occur more slowly or more quickly in certain conditions, choices between two tissue states (e.g. gonad type) can be modified by environmental factors, etc.
Exploratory processes are search and find processes like following a chemical cue gradient to a point source. We see this type of process in development when we examine how axons form during neurogenesis and how vasculature arises to feed organs and tissues. We see it in adults in the vertebrate adaptive immune system and foraging behavior in chemically-guided organisms like ants. We say that this type of process shows robustness because it adapts quickly to local environmental changes. For example, with strict XY grid patterning of vasculature, growth over developmental time would need to be under strict control and size/shape variance in organs would not be tolerated. Small blood vessels, however, do not grow due to a coordinate system, rather they grow based on a "supply and demand" system with outgrowths to regions of low oxygen. Cells secrete a protein signal (VEGF) when they are low on oxygen, promoting blood vessel growth towards them2.
Exploratory processes are also adaptable over evolutionary time since they allow for size and shape variance. This is important within populations, where individuals may vary in size or shape. But it is also important over longer periods of evolutionary time as these flexible patterning processes will form a useable system based on their simple set of rules for growth. For example, transplanted leg discs in insects become innervated as do ectopic limbs in chick embryos3,4. In this way, exploratory processes facilitate evolution by helping to build a viable body when other morphological components have evolved into more fit conformations.
In plants, the ability to separate the the light reactions from the Calvin Cycle of photosynthesis either temporally (as in CAM plants) or spatially (as in C4 plants) has lead to incredible success and diversity in these plant types as they are no longer reliant on keeping their stomata open during the hottest and dryest (but also sunniest) parts of the day. In our own cells, we can see compartmentalization of our mitochondria, with the intermembrane space about 10 times more acidic than the lumen. This allows for the proton motive force to be concentrated and also protects the pH of the rest of the cell. Our cells also physically separate cell-cell signaling from transcriptional regulation - allowing modification of signaling pathways dependent on cell history (development) and environment.
When one compartment of an organism (or cell) can act semi-independently of another, we expect higher variation. That is, each compartment can run its developmental program via activation and inhibition of specific GRNs without disrupting the development of other compartments. In this way, gene expression changes that affect only one or a few compartments might be limited in affect. Evolution thus may be able to act on compartments individually, as long as these are expression changes like transcript number, protein isoforms, or post-translational modification. Protein-coding mutations, on the other hand, could potentially act on many compartments at once. Evolution can potentially act on individual compartments via gene expression changes, while exploratory processes can maintain the robustness of signaling and nutrient pathways across the entire body.
Evolvability in animals relies on two competing types of development:
- Processes resistant to evolutionary change. These include exploratory processes that use external signals to find the most efficient or most effective morphology, leading to retention of the process of. But these can also include processes that are conserved over long evolutionary periods of time due to physical or genetic constraints.
- Changable processes. These include processes that change over time because they are either compartmentalized or are co-opted onto other robust developmental programs. Compartmentation (a process resistant to change) allows for physical separation of developmental processes, and weak regulatory linkage allows for co-option of processes to new times and places (for example compartments).
In this way, evolutionary change happens on a background of robust processes. Some of these robust processes are malleable in developmental time (like vascularization), while others are constraints - limiting what is possible in a particular evolutionary lineage. One example we have already considered is tetrapod limb evolution. While there are physical and genetic constraints on this limiting the number of bone condensations per developmental section, these constraints also create compartments - the stylopod, zeugopod, and autopod as well as the 5 digits. Size variation and adaptations to the compartments is supported by robust exploratory processes, linking bone development to supporting musculature, vasculature, and innervation.
- "The Theory of Facilitated Variation" 2007, PNAS, John Gerhart and Marc Kirschner, https://doi.org/10.1073/pnas.0701035104
- Reviewed in "Hypoxia-Induced Angiogenesis: Good and Evil," 2011, Genes and Cancer, Bryan L. Krock, Nicolas Skuli. and M. Celeste Simon doi: 10.1177/1947601911423654
- "Axonal projections from transplanted ectopic legs in an insect," 1985, Journal of Comparative Neurology, P. Sivasubramanian D. R. Nässel, doi.org/10.1002/cne.902390211
- "The innervation of FGF-induced additional limbs in the chick embryo," 2003, Journal of Anatomy, BW Turney, AM Rowan-Hull, and JM Brown doi: 10.1046/j.1469-7580.2003.00131.x
- "Angiogenesis: An Adaptive Dynamic Biological Patterning Problem," 2013, PLoS Computational Biology, Timothy W. Secomb , Jonathan P. Alberding, Richard Hsu, Mark W. Dewhirst, Axel R. Pries https://doi.org/10.1371/journal.pcbi.1002983
- "Neuronal migration and lamination in the vertebrate retina," 2018, Frontiers in Neuroscience, Rana Amini, Mauricio Rocha-Martins, and Caren Norden. doi: 10.3389/fnins.2017.00742
Thumbnail is a graph of standing variation in a population (10,000 polymorphic sites from Human Chromosome 1) by Graham Coop, published on Wikimedia Commons under a CC BY 3.0 license.
Is evolvability evolvable?
In recent years, biologists have increasingly been asking whether the ability to evolve — the evolvability — of biological systems, itself evolves, and whether this phenomenon is the result of natural selection or a by-product of other evolutionary processes. The concept of evolvability, and the increasing theoretical and empirical literature that refers to it, may constitute one of several pillars on which an extended evolutionary synthesis will take shape during the next few years, although much work remains to be done on how evolvability comes about.
Phenotypic plasticity in plants includes the timing of transition from vegetative to reproductive growth stage, the allocation of more resources to the roots in soils that contain low concentrations of nutrients, the size of the seeds an individual produces depending on the environment,  and the alteration of leaf shape, size, and thickness.  Leaves are particularly plastic, and their growth may be altered by light levels. Leaves grown in the light tend to be thicker, which maximizes photosynthesis in direct light and have a smaller area, which cools the leaf more rapidly (due to a thinner boundary layer). Conversely, leaves grown in the shade tend to be thinner, with a greater surface area to capture more of the limited light.   Dandelion are well known for exhibiting considerable plasticity in form when growing in sunny versus shaded environments. The transport proteins present in roots also change depending on the concentration of the nutrient and the salinity of the soil.  Some plants, Mesembryanthemum crystallinum for example, are able to alter their photosynthetic pathways to use less water when they become water- or salt-stressed. 
Because of phenotypic plasticity, it is hard to explain and predict the traits when plants are grown in natural conditions unless an explicit environment index can be obtained to quantify environments. Identification of such explicit environment indices from a critical growth periods being highly correlated with sorghum and rice flowering time enables such predictions.  
Phytohormones and leaf plasticity Edit
Leaves are very important to a plant in that they create an avenue where photosynthesis and thermoregulation can occur. Evolutionarily, the environmental contribution to leaf shape allowed for a myriad of different types of leaves to be created.  Leaf shape can be determined by both genetics and the environment.  Environmental factors, such as light and humidity, have been shown to affect leaf morphology,  giving rise to the question of how this shape change is controlled at the molecular level. This means that different leaves could have the same gene but present a different form based on environmental factors. Plants are sessile, so this phenotypic plasticity allows the plant to take in information from its environment and respond without changing its location.
In order to understand how leaf morphology works, the anatomy of a leaf must be understood. The main part of the leaf, the blade or lamina, consists of the epidermis, mesophyll, and vascular tissue. The epidermis contains stomata which allows for gas exchange and controls perspiration of the plant. The mesophyll contains most of the chloroplast where photosynthesis can occur. Developing a wide blade/lamina can maximize the amount of light hitting the leaf, thereby increasing photosynthesis, however too much sunlight can damage the plant. Wide lamina can also catch wind easily which can cause stress to the plant, so finding a happy medium is imperative to the plants’ fitness. The Genetic Regulatory Network is responsible for creating this phenotypic plasticity and involves a variety of genes and proteins regulating leaf morphology. Phytohormones have been shown to play a key role in signaling throughout the plant, and changes in concentration of the phytohormones can cause a change in development. 
Studies on the aquatic plant species Ludwigia arcuata have been done to look at the role of abscisic acid (ABA), as L. arcuata is known to exhibit phenotypic plasticity and has two different types of leaves, the aerial type (leaves that touch the air) and the submerged type (leaves that are underwater).  When adding ABA to the underwater shoots of L. arcuata, the plant was able to produce aerial type leaves underwater, suggesting that increased concentrations of ABA in the shoots, likely caused by air contact or a lack of water, triggers the change from the submerged type of leaf to the aerial type. This suggests ABA's role in leaf phenotypic change and its importance in regulating stress through environmental change (such as adapting from being underwater to above water). In the same study, another phytohormone, ethylene, was shown to induce the submerged leaf phenotype unlike ABA, which induced aerial leaf phenotype. Because ethylene is a gas, it tends to stay endogenously within the plant when underwater – this growth in concentration of ethylene induces a change from aerial to submerged leaves and has also been shown to inhibit ABA production, further increasing the growth of submerged type leaves. These factors (temperature, water availability, and phytohormones) contribute to changes in leaf morphology throughout a plants lifetime and are vital to maximize plant fitness.
The developmental effects of nutrition and temperature have been demonstrated.  The gray wolf (Canis lupus) has wide phenotypic plasticity.   Additionally, male speckled wood butterflies have two morphs: one with three dots on its hindwing, and one with four dots on its hindwings. The development of the fourth dot is dependent on environmental conditions – more specifically, location and the time of year.  In amphibians, Pristimantis mutabilis has remarkable phenotypic plasticity.  Another example is the southern rockhopper penguin.  Rockhopper penguins are present at a variety of climates and locations Amsterdam Island's subtropical waters, Kerguelen Archipelago's subarctic coastal waters, and Crozet Archipelago's subantarctic coastal waters.  Due to the species plasticity they are able to express different strategies and foraging behaviors depending on the climate and environment.  A main factor that has influenced the species' behavior is where food is located. 
Plastic responses to temperature are essential among ectothermic organisms, as all aspects of their physiology are directly dependent on their thermal environment. As such, thermal acclimation entails phenotypic adjustments that are found commonly across taxa, such as changes in the lipid composition of cell membranes. Temperature change influences the fluidity of cell membranes by affecting the motion of the fatty acyl chains of glycerophospholipids. Because maintaining membrane fluidity is critical for cell function, ectotherms adjust the phospholipid composition of their cell membranes such that the strength of van der Waals forces within the membrane is changed, thereby maintaining fluidity across temperatures. 
Phenotypic plasticity of the digestive system allows some animals to respond to changes in dietary nutrient composition,   diet quality,   and energy requirements.   
Changes in the nutrient composition of the diet (the proportion of lipids, proteins and carbohydrates) may occur during development (e.g. weaning) or with seasonal changes in the abundance of different food types. These diet changes can elicit plasticity in the activity of particular digestive enzymes on the brush border of the small intestine. For example, in the first few days after hatching, nestling house sparrows (Passer domesticus) transition from an insect diet, high in protein and lipids, to a seed based diet that contains mostly carbohydrates this diet change is accompanied by two-fold increase in the activity of the enzyme maltase, which digests carbohydrates.  Acclimatizing animals to high protein diets can increase the activity of aminopeptidase-N, which digests proteins.  
Poor quality diets (those that contain a large amount of non-digestible material) have lower concentrations of nutrients, so animals must process a greater total volume of poor-quality food to extract the same amount of energy as they would from a high-quality diet. Many species respond to poor quality diets by increasing their food intake, enlarging digestive organs, and increasing the capacity of the digestive tract (e.g. prairie voles,  Mongolian gerbils,  Japanese quail,  wood ducks,  mallards  ). Poor quality diets also result in lower concentrations of nutrients in the lumen of the intestine, which can cause a decrease in the activity of several digestive enzymes. 
Animals often consume more food during periods of high energy demand (e.g. lactation or cold exposure in endotherms), this is facilitated by an increase in digestive organ size and capacity, which is similar to the phenotype produced by poor quality diets. During lactation, common degus (Octodon degus) increase the mass of their liver, small intestine, large intestine and cecum by 15–35%.  Increases in food intake do not cause changes in the activity of digestive enzymes because nutrient concentrations in the intestinal lumen are determined by food quality and remain unaffected.  Intermittent feeding also represents a temporal increase in food intake and can induce dramatic changes in the size of the gut the Burmese python (Python molurus bivittatus) can triple the size of its small intestine just a few days after feeding. 
AMY2B (Alpha-Amylase 2B) is a gene that codes a protein that assists with the first step in the digestion of dietary starch and glycogen. An expansion of this gene in dogs would enable early dogs to exploit a starch-rich diet as they fed on refuse from agriculture. Data indicated that the wolves and dingo had just two copies of the gene and the Siberian Husky that is associated with hunter-gatherers had just three or four copies, whereas the Saluki that is associated with the Fertile Crescent where agriculture originated had 29 copies. The results show that on average, modern dogs have a high copy number of the gene, whereas wolves and dingoes do not. The high copy number of AMY2B variants likely already existed as a standing variation in early domestic dogs, but expanded more recently with the development of large agriculturally based civilizations. 
Infection with parasites can induce phenotypic plasticity as a means to compensate for the detrimental effects caused by parasitism. Commonly, invertebrates respond to parasitic castration or increased parasite virulence with fecundity compensation in order to increase their reproductive output, or fitness. For example, water fleas (Daphnia magna), exposed to microsporidian parasites produce more offspring in the early stages of exposure to compensate for future loss of reproductive success.  A reduction in fecundity may also occur as a means of re-directing nutrients to an immune response,  or to increase longevity of the host.  This particular form of plasticity has been shown in certain cases to be mediated by host-derived molecules (e.g. schistosomin in snails Lymnaea stagnalis infected with trematodes Trichobilharzia ocellata) that interfere with the action of reproductive hormones on their target organs.  Changes in reproductive effort during infection is also thought to be a less costly alternative to mounting resistance or defence against invading parasites, although it can occur in concert with a defence response. 
Hosts can also respond to parasitism through plasticity in physiology aside from reproduction. House mice infected with intestinal nematodes experience decreased rates of glucose transport in the intestine. To compensate for this, mice increase the total mass of mucosal cells, cells responsible for glucose transport, in the intestine. This allows infected mice to maintain the same capacity for glucose uptake and body size as uninfected mice. 
Phenotypic plasticity can also be observed as changes in behaviour. In response to infection, both vertebrates and invertebrates practice self-medication, which can be considered a form of adaptive plasticity.  Various species of non-human primates infected with intestinal worms engage in leaf-swallowing, in which they ingest rough, whole leaves that physically dislodge parasites from the intestine. Additionally, the leaves irritate the gastric mucosa, which promotes the secretion of gastric acid and increases gut motility, effectively flushing parasites from the system.  The term "self-induced adaptive plasticity" has been used to describe situations in which a behavior under selection causes changes in subordinate traits that in turn enhance the ability of the organism to perform the behavior.  For example, birds that engage in altitudinal migration might make "trial runs" lasting a few hours that would induce physiological changes that would improve their ability to function at high altitude. 
Woolly bear caterpillars (Grammia incorrupta) infected with tachinid flies increase their survival by ingesting plants containing toxins known as pyrrolizidine alkaloids. The physiological basis for this change in behaviour is unknown however, it is possible that, when activated, the immune system sends signals to the taste system that trigger plasticity in feeding responses during infection. 
The red-eyed tree frog, Agalychnis callidryas, is an arboreal frog (hylid) that resides in the tropics of Central America. Unlike many frogs, the red-eyed tree frog has arboreal eggs which are laid on leaves hanging over ponds or large puddles and, upon hatching, the tadpoles fall into the water below. One of the most common predators encountered by these arboreal eggs is the cat-eyed snake, Leptodeira septentrionalis. In order to escape predation, the red-eyed tree frogs have developed a form of adaptive plasticity, which can also be considered phenotypic plasticity, when it comes to hatching age the clutch is able to hatch prematurely and survive outside of the egg five days after oviposition when faced with an immediate threat of predation. The egg clutches take in important information from the vibrations felt around them and use it to determine whether or not they are at risk of predation. In the event of a snake attack, the clutch identifies the threat by the vibrations given off which, in turn, stimulates hatching almost instantaneously. In a controlled experiment conducted by Karen Warkentin, hatching rate and ages of red-eyed tree frogs were observed in clutches that were and were not attacked by the cat-eyed snake. When a clutch was attacked at six days of age, the entire clutch hatched at the same time, almost instantaneously. However, when a clutch is not presented with the threat of predation, the eggs hatch gradually over time with the first few hatching around seven days after oviposition, and the last of the clutch hatching around day ten. Karen Warkentin's study further explores the benefits and trade-offs of hatching plasticity in the red-eyed tree frog. 
Plasticity is usually thought to be an evolutionary adaptation to environmental variation that is reasonably predictable and occurs within the lifespan of an individual organism, as it allows individuals to 'fit' their phenotype to different environments.   If the optimal phenotype in a given environment changes with environmental conditions, then the ability of individuals to express different traits should be advantageous and thus selected for. Hence, phenotypic plasticity can evolve if Darwinian fitness is increased by changing phenotype.   A similar logic should apply in artificial evolution attempting to introduce phenotypic plasticity to artificial agents.  However, the fitness benefits of plasticity can be limited by the energetic costs of plastic responses (e.g. synthesizing new proteins, adjusting expression ratio of isozyme variants, maintaining sensory machinery to detect changes) as well as the predictability and reliability of environmental cues  (see Beneficial acclimation hypothesis).
Freshwater snails (Physa virgata), provide an example of when phenotypic plasticity can be either adaptive or maladaptive. In the presence of a predator, bluegill sunfish, these snails make their shell shape more rotund and reduce growth. This makes them more crush-resistant and better protected from predation. However, these snails cannot tell the difference in chemical cues between the predatory and non-predatory sunfish. Thus, the snails respond inappropriately to non-predatory sunfish by producing an altered shell shape and reducing growth. These changes, in the absence of a predator, make the snails susceptible to other predators and limit fecundity. Therefore, these freshwater snails produce either an adaptive or maladaptive response to the environmental cue depending on whether the predatory sunfish is actually present.  
Given the profound ecological importance of temperature and its predictable variability over large spatial and temporal scales, adaptation to thermal variation has been hypothesized to be a key mechanism dictating the capacity of organisms for phenotypic plasticity.  The magnitude of thermal variation is thought to be directly proportional to plastic capacity, such that species that have evolved in the warm, constant climate of the tropics have a lower capacity for plasticity compared to those living in variable temperate habitats. Termed the "climatic variability hypothesis", this idea has been supported by several studies of plastic capacity across latitude in both plants and animals.   However, recent studies of Drosophila species have failed to detect a clear pattern of plasticity over latitudinal gradients, suggesting this hypothesis may not hold true across all taxa or for all traits.  Some researchers propose that direct measures of environmental variability, using factors such as precipitation, are better predictors of phenotypic plasticity than latitude alone. 
Selection experiments and experimental evolution approaches have shown that plasticity is a trait that can evolve when under direct selection and also as a correlated response to selection on the average values of particular traits. 
Unprecedented rates of climate change are predicted to occur over the next 100 years as a result of human activity.  Phenotypic plasticity is a key mechanism with which organisms can cope with a changing climate, as it allows individuals to respond to change within their lifetime.  This is thought to be particularly important for species with long generation times, as evolutionary responses via natural selection may not produce change fast enough to mitigate the effects of a warmer climate.
The North American red squirrel (Tamiasciurus hudsonicus) has experienced an increase in average temperature over this last decade of almost 2 °C. This increase in temperature has caused an increase in abundance of white spruce cones, the main food source for winter and spring reproduction. In response, the mean lifetime parturition date of this species has advanced by 18 days. Food abundance showed a significant effect on the breeding date with individual females, indicating a high amount of phenotypic plasticity in this trait. 
We employed the Virtual Cell (VC) model [21, 22] (Fig. 1) to study the evolution of adaptive strategies to cope with repeated environmental change. VCs exist in populations of fixed size and compete for a chance to produce offspring in the next generation, completely replacing the current population. Their fitness depends on the ability to maintain cellular homeostasis. Cells have a high fitness if they maintain equilibrium concentrations of the two internal molecule species A and X close to a fixed target during fluctuations in external resource (A) concentration that range over more than two orders of magnitude. Concentrations of A and X arise from the internal cellular dynamics that are given by a system of ODEs, representing the activities of the proteins in the cell. The activities of catabolic and anabolic enzymes and pumps directly affect concentrations of A and X. Transcription factors (TFs) influence gene expression when their binding motif matches a binding site in the operator of a gene. TFs can bind either A or X as a ligand, and have a differential regulatory effect on their downstream genes, depending on their ligand binding state. This ability to regulate gene expression depending on ligand binding state is crucial for the cells’ capacity to evolve homeostasis.
Virtual Cell model overview. a Virtual Cells have a circular genome that encodes metabolic and regulatory proteins. An externally available resource molecule (A) diffuses passively over the membrane (1) and is actively imported (2) by pump proteins. Once inside, A is converted to (X) by catabolic enzymes. X serves as the energy source for the import reaction (2). In addition, A and X are converted to an unspecified end product (4) by anabolic enzymes. Protein expression from genes (5) can be regulated by TFs if their binding motif matches the gene’s operator sequence. Binding of a ligand (A or X) by the TF alters its regulatory effect on gene expression. The genome can contain multiple copies of any of the gene types. Different copies may encode different values of the gene’s parameters, such as the enzymatic constants of the reaction that they catalyse or the binding motif and regulatory effect. b Fitness is determined by measuring the difference (Δ) between the realised steady state concentrations of internal A and X and the homeostasis target value (dotted line). c During the evolutionary experiments the external concentration of A is continually varying, while the homeostasis target remains constant. Cells have a chance proportional to their fitness to contribute offspring to the next generation
All proteins are transcribed from a spatially explicit, circular genome. Point mutations affect parameters of individual genes, such as the kinetic constants of enzymes, operator binding sites, and binding motifs and regulatory effect parameters of TFs. Large scale mutation events are the duplication, deletion or translocation of stretches of neighbouring genes as well as whole genome duplications (WGD). After duplicating, the two identical copies of a gene will diverge due to subsequent, independently accumulating point mutations. We are interested in the genome structure and mutational events on the line of descent (LOD) of a lineage (see “Constructing the line of descent” in “Methods”). In most of the analysis we focus on the mutational events fixed shortly before and after environmental change.
Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves
The structure of compound leaves provides flexibility for morphological change by variation in the shapes, sizes and arrangement of leaflets. Here, we conduct a multilevel analysis of shape variation in compound leaves to explore the developmental plasticity and evolutionary potential that are the basis of diversification in leaf shape. We use the methods of geometric morphometrics to study the shapes of individual leaflets and whole leaves in 20 taxa of Potentilla (sensu lato). A newly developed test based on the bootstrap approach suggests that uncertainty in the molecular phylogeny precludes firm conclusions whether there is a phylogenetic signal in the data on leaf shape. For variation among taxa, variation within taxa, as well as fluctuating asymmetry, there is evidence of strong morphological integration. The patterns of variation are similar across all three levels, suggesting that integration within taxa may act as a constraint on evolutionary change.
© 2011 The Authors. Journal of Evolutionary Biology © 2011 European Society For Evolutionary Biology.
Scanning procedures in chimpanzees were approved by the Institutional Animal Care and Use Committee of Emory University, and human subjects participated in scan acquisition in accordance with guidelines of the Washington University Human Studies Committee.
We are grateful to Emiliano Bruner for general advice and orientation, to Eran Shifferman and Gerard Muntané for commenting on earlier versions of the manuscript and to David Polly and David Sánchez-Martín for their invaluable ideas for graphical representations of brain surface models. This work was supported by National Science Foundation grant nos. BCS-0515484, BCS-0549117, BCS-0824531 and DGE-0801634 National Institutes of Health grant nos. HD-56232, MH-92932, NS-42867, NS-73134, RR-00165 and U01 MH081896 and James S. McDonnell Foundation grant nos. 22002078, 220020165 and 220020293. The Open Access Series of Imaging Studies (OASIS) project is supported by grants P50 AG05681, P01 AG03991, R01 AG021910, P50 MH071616, U24 RR021382 and R01 MH56584.
Conclusion and prospectus
The advent of molecular, genomic and bioinformatic techniques and their increasing applicability to diverse species has enormously enhanced experimental biologists' ability to understand `how animals work'(Schmidt-Nielsen, 1972). Adaptational biology will be incomplete, however, until the understanding of how adaptations came into being is equally advanced. This understanding may well come about through sustained interaction with modern evolutionary biologists, evolutionary genomicists and evolutionary systems biologists. One clear outcome of such interaction is that single-nucleotide mutation, often the mainstay of adaptational biologists' evolutionary thinking, will become viewed as only one of several mechanisms in evolution's toolkit. The other mechanisms may be far more powerful than single-nucleotide mutation in facilitating evolvability and, although they have not done so yet, be able to explain in detail the origin of the complex traits that fascinate adaptational biologists.