Developmental Noise Research Articles

Developmental noise, entropy, and biological system condition.

Developmental noise is considered as a permissible level of entropy, as a compromise between the cost and needed precision of the realization of genetic information. In terms of entropy, noise is a measure of acceptable level of disorder to ensure a reliable system operation. Developmental noise plays a role in the observed phenotypic diversity and is associated with other indicators of the biological system condition. The thermodynamic characteristic of entropy by the energy metabolism also turns out to be related to the developmental noise. Phenotypic variability is largely determined by developmental homeostasis, including both canalization (an ability to form a similar phenotype under different conditions) and developmental stability (a capability for perfect development measured by noise level). It is shown that the change in the noise level, as an expression of the certain entropy level, unlike other forms of phenotypic variability, is a reflection of a change in the system condition. Although the entropy indices of ontogeny and community under certain conditions can change simultaneously, the entropy index at the level of developmental noise proves to be a more unambiguous and universal measure of the disorder of a biological system, compared to biodiversity indices at the community level.

The genetics of phenotypic plasticity. XVIII. Developmental limits restrict adaptive plasticity.

After environmental change, the trait evolution needed to rescue a population depends on the functional form of the plastic change (reaction norm) of that trait. Nearly all previous models of plasticity evolution for continuous traits have assumed that the functional form is linear, i.e., no limits on the range of plasticity. This paper examines the effect of developmental limits, modeled as a sigmoidal reaction norm, on evolutionary rescue after an abrupt environmental change and the subsequent evolution of plasticity, including genetic assimilation. We examined four different scenarios: (1) developmental limits only, (2) developmental limits plus a cost of plasticity, (3) developmental limits with developmental noise, and (4) developmental limits plus environmental variation. The probability of evolutionary rescue increased with an increase in phenotypic variation allowed by plastic development. With a smaller limit to the range of the plastic phenotype, the evolution of adaptive plasticity was limited, meaning the evolution of non-plastic genes was necessary. The addition of developmental constraints to the model did not speed up genetic assimilation, suggesting new theory is needed to understand empirical observations. The modeling framework presented here could be extended to different ecological and evolutionary conditions, alternative reaction norm shapes, the evolution of additional reaction norm parameters such as the range or the location of the inflection point on the environmental axis, or other function-valued traits.

Intensive agriculture increases fluctuating asymmetry of dorsal head shape in Iberian asp viper populations

AbstractHabitats resulting from agricultural intensification harbour a wide array of stressors for resident organisms. Environmental stress during development can leave imprints on the phenotype that are useful as indicators of its impairment. Among them, fluctuating asymmetry (FA), considered the morphological manifestation of developmental instability (DI), may reflect the increment of developmental noise and the inefficiency of buffering mechanisms. Here, we evaluated for the first time the impact of intensive agriculture on the development of a viviparous reptile, the asp viper, Vipera aspis (Linnaeus 1758), by means of FA. To this end, we first quantified unsigned asymmetry indexes (uAI) of dorsal head shape captured by geometric morphometrics (GM) and of seven pholidotic traits in 127 and 482 individuals, respectively. Using linear models, we then tested for variation in uAI according to habitat type. Furthermore, we tested the effect of climatic variables with a potential influence on development, and thus, on FA. We performed analyses at the V. aspis zinnikeri subspecies range and at the population level, including three well‐sampled natural localities (NAT) and three sites of intensive agriculture (AGR). We found significantly higher FA levels in dorsal head shape in individuals from agricultural habitats than in those from natural habitats, which suggests that asp viper development is impaired by stressors resulting from agricultural intensification. Our results also point to a lower sensitivity of traditional morphological tools to capture the signal that intensive agriculture leaves on development and a lack of capacity of climatic factors in isolation to predict variation in the degree of asymmetry. In addition to encouraging the use of high‐precision methods, we hypothesize on the overall effect of different stressors linked to intensive agriculture as the real constraint.

Emergence of phenotypic plasticity through epigenetic mechanisms.

Plasticity is found in all domains of life and is particularly relevant when populations experience variable environmental conditions. Traditionally, evolutionary models of plasticity are non-mechanistic: they typically view reactions norms as the target of selection, without considering the underlying genetics explicitly. Consequently, there have been difficulties in understanding the emergence of plasticity, and in explaining its limits and costs. In this paper, we offer a novel mechanistic approximation for the emergence and evolution of plasticity. We simulate random "epigenetic mutations" in the genotype-phenotype mapping, of the kind enabled by DNA-methylations/demethylations. The frequency of epigenetic mutations at loci affecting the phenotype is sensitive to organism stress (trait-environment mismatch), but is also genetically determined and evolvable. Thus, the "random motion" of epigenetic markers enables developmental learning-like behaviors that can improve adaptation within the limits imposed by the genotypes. However, with random motion being "goal-less," this mechanism is also vulnerable to developmental noise leading to maladaptation. Our individual-based simulations show that epigenetic mutations can hide alleles that are temporarily unfavorable, thus enabling cryptic genetic variation. These alleles can be advantageous at later times, under regimes of environmental change, in spite of the accumulation of genetic loads. Simulations also demonstrate that plasticity is favored by natural selection in constant environments, but more under periodic environmental change. Plasticity also evolves under directional environmental change as long as the pace of change is not too fast and costs are low.

Developmental hourglass: Verification by numerical evolution and elucidation by dynamical-systems theory.

Determining the general laws between evolution and development is a fundamental biological challenge. Developmental hourglasses have attracted increased attention as candidates for such laws, but the necessity of their emergence remains elusive. We conducted evolutionary simulations of developmental processes to confirm the emergence of the developmental hourglass and unveiled its establishment. We considered organisms consisting of cells containing identical gene networks that control morphogenesis and evolved them under selection pressure to induce more cell types. By computing the similarity between the spatial patterns of gene expression of two species that evolved from a common ancestor, a developmental hourglass was observed, that is, there was a correlation peak in the intermediate stage of development. The fraction of pleiotropic genes increased, whereas the variance in individuals decreased, consistent with previous experimental reports. Reduction of the unavoidable variance by initial or developmental noise, essential for survival, was achieved up to the hourglass bottleneck stage, followed by diversification in developmental processes, whose timing is controlled by the slow expression dynamics conserved among organisms sharing the hourglass. This study suggests why developmental hourglasses are observed within a certain phylogenetic range of species.

Developmental noise and phenotypic plasticity are correlated in Drosophila simulans.

Non-genetic variation is the phenotypic variation induced by the differential expression of a genotype in response to varying environmental cues and is broadly categorized into two types: phenotypic plasticity and developmental noise. These aspects of variation have been suggested to play an important role in adaptive evolution. However, the mechanisms by which these two types of non-genetic variations influence the evolutionary process are currently poorly understood. Using a machine-learning-based phenotyping tool, we independently quantified phenotypic plasticity and developmental noise in the wing morphological traits of the fruit fly Drosophila simulans. Utilizing a rearing experiment, we demonstrated plastic responses in both wing size and shape as well as non-zero heritability of both phenotypic plasticity and developmental noise, which suggests that adaptive phenotypic plasticity can evolve via genetic accommodation in the wing morphology of D. simulans. We found a positive correlation between phenotypic plasticity and developmental noise, while the correlation between the plastic response to three kinds of environmental factors that were examined (nutrient condition, temperature, and light-dark cycle) was poor. These results suggest that phenotypic plasticity and developmental noise contribute to evolvability in a similar manner, however, the mechanisms that underlie the correspondence between these two types of variation remain to be elucidated.

No association between developmental instability as a general measure of stress and 2D:4D digit ratios in a non-western sample.

Random deviation from perfect symmetry of organisms is defined as fluctuating asymmetry. Fluctuating asymmetry is widely considered to be a marker of developmental instability, developmental noise and phenotypic quality at the population level. In this study, we investigated hypothesized relationship between 2D:4D digit ratios as a proxy measure of prenatal sex hormones and developmental instability levels in young adult humans. In the study, seven bilateral traits were measured for fluctuating asymmetry, as well as second and fourth digit lengths on both hands of 185 individuals, 87 men (mean age: 22.42 ± 3.37) and 97 women (mean age: 22.88 ± 3.87). The second digit length was divided by the fourth digit length and the resulting value was used as the digit ratio (2D:4D). Composite fluctuating asymmetry was calculated using five bilateral traits displaying fluctuating asymmetry. Only the right hand 2D:4D ratio is lower in men than in women. However, this difference disappears when the effect of digit lengths is controlled. Composite fluctuating asymmetry results reveal that men are more asymmetrical than women. There was no significant relationship between digit ratios and composite fluctuating asymmetry. In this study, the 2D:4D digit ratios appear to be influenced (at least in humans) by different digit lengths. This study also confirms previous studies that digit ratios as a proxy measure of exposure to either high testosterone or estrogen levels during early development does not appear to affect levels of developmental instability.

Developmental Noise and Biological System Condition: Prolegomena

Developmental noise is a variety that is not related to the usually distinguished sources of phenotypic diversity, i.e., differences in the genotype and in the environment. This variation arises in the process of the realization of genetic information and reflects the imperfection of ontogenetic processes. The most common measure of it is the value of fluctuating asymmetry as slight deviations from the symmetry. Developmental noise proves to be one of the main sources of intrapopulation phenotypic diversity. The magnitude of this variability is an ontogenetic response to environmental or genetic stress, and its assessment, in fact, provides a unique opportunity to estimate the developing system condition. The level of developmental noise, characterizing an organism’s condition, acts as another population parameter that allows to approach the evaluation of the community condition. Initial deviations in the system condition can be detected even against the background of optimal estimates of abundance, biodiversity, and ecosystem functioning.

A Dilp8-dependent time window ensures tissue size adjustment in Drosophila.

The control of organ size mainly relies on precise autonomous growth programs. However, organ development is subject to random variations, called developmental noise, best revealed by the fluctuating asymmetry observed between bilateral organs. The developmental mechanisms ensuring bilateral symmetry in organ size are mostly unknown. In Drosophila, null mutations for the relaxin-like hormone Dilp8 increase wing fluctuating asymmetry, suggesting that Dilp8 plays a role in buffering developmental noise. Here we show that size adjustment of the wing primordia involves a peak of dilp8 expression that takes place sharply at the end of juvenile growth. Wing size adjustment relies on a cross-organ communication involving the epidermis as the source of Dilp8. We identify ecdysone signaling as both the trigger for epidermal dilp8 expression and its downstream target in the wing primordia, thereby establishing reciprocal hormonal feedback as a systemic mechanism, which controls organ size and bilateral symmetry in a narrow developmental time window.

Anthropometric fluctuating asymmetries in living humans through the eyes of an anthropologist.

There are many environmental and genetic factors that disrupt the stable structure of development in organisms. Although the strength of these vary, they leave certain signs in the body structure. Fluctuating asymmetry is a widely used population-level index of developmental instability, developmental noise, and robustness. Many bilateral traits are used in fluctuating asymmetry studies in humans. These traits include dermatoglyphics, limb lengths and widths, bilateral facial characters, and teeth. In this review, I evaluate the measurement methods of many bilateral anthropometric characters, taken from the bodies of living individuals with classical digital calipers.

Developmental noise is an overlooked contributor to innate variation in psychological traits.

Stochastic developmental variation is an additional important source of variance - beyond genes and environment - that should be included in considering how our innate psychological predispositions may interact with environment and experience, in a culture-dependent manner, to ultimately shape patterns of human behaviour.

Random Developmental Variation of Human Phenotypic Traits, as Estimated by Fluctuating Asymmetry and Twin Studies

Random developmental variation, or developmental noise, contributes to total phenotypic variation in the human species. Despite exhortations to examine it, especially with respect to human behavior and intelligence, there has been little research specifically devoted to doing so. Random developmental variation can be estimated in studies of fluctuating asymmetry and comparisons of monozygotic and dizygotic twins. Estimation of random developmental variation requires that both genotype and environment be held constant. In a small sample of bilaterally symmetrical traits (dermatoglyphic ridge counts, digit lengths, ear lengths and widths), I show how the random developmental component can be estimated. In these traits, the percentage of total phenotypic variation attributable to developmental noise ranges from 3 percent to more than 25 percent. Moreover, for dermatoglyphic ridge counts, fluctuating asymmetry and twin comparisons give essentially the same estimates.

Distinguishing between unreliability and dishonesty: A comparative study of aggressive communication in crayfish

Abstract A major challenge in the study of animal communication is distinguishing whether signals convey honest or dishonest information. Biologists infer the honesty of a signal from its correlation with the information being signalled (e.g. fecundity or fighting ability)—the better the correlation, the more honest the signal. However, this view of signalling potentially conflates unreliable indicators with dishonest signals. Just because a trait conveys unreliable information does not mean that the structure serves as a dishonest signal; developmental noise, genetic drift and environmental constraints can reduce the covariation between a putative signal and an organism's quality. Moreover, a trait must influence the behaviour of other organisms to qualify as a signal. We studied how a putative signal, claw size, affects physical performance and social dominance in three species of stream‐dwelling crayfish, which fight routinely over resources. For comparison, we measured the relationship between claw size and claw strength in three species of burrowing crayfish, which do not fight. In all species, crayfish with larger claws were not necessarily stronger, indicating that claw size poorly indicates claw strength. However, claw size is unlikely to function as a dishonest signal of fighting ability in these species for two reasons. First, claw size unreliably indicates claw strength in both the stream‐dwelling species and the burrowing species. Second, relative claw size poorly predicted whether stream‐dwelling crayfish would escalate aggression, questioning whether claw size serves as a signal. Instead, stream‐dwelling crayfish escalated aggression based on their relative body size. Our results highlight the importance of observing behaviour when determining the honesty of a signal. As such, future studies must distinguish between phenotypes that are unreliable indicators (or reliable indicators) from phenotypes that have been selected for dishonest (or honest) signalling. A free Plain Language Summary can be found within the Supporting Information of this article.

Phenotypic plasticity and developmental noise in hybrid and parental clones of Daphnia longispina complex

According to the “temporal hybrid superiority hypothesis”, seasonal variability in environmental factors in temperate lakes gives hybrid clones within the D. longispina complex a temporary fitness advantage, thus allowing long-term, dynamic coexistence of hybrids and maternal taxa. However, the maintenance of hybrids would not require their superiority under any given set of environmental conditions if their average fitness over longer periods surpassed that of more specialized and less flexible parental clones. Phenotypic plasticity and developmental noise of several hybrid and maternal clones of Daphnia (Daphnia galeata, Daphnia hyalina, their hybrids and backcrosses) were compared in a series of laboratory experiments. Changes in depth selection and body size at first reproduction were scored in Daphnia exposed to predator (planktivorous fish) threat, to the presence of filamentous cyanobacteria (Cylindrospermopsis raciborskii), and to the presence of toxic compounds (PCB52 and PCB153). The hybrid clones were found to exhibit the broadest phenotypic plasticity of the studied traits in response to the different stress factors. Developmental noise in depth selection behaviour was the lowest in Daphnia galeata, the highest in Daphnia hyalina, and intermediate in hybrid and backcross clones. This diversity of reaction norms might permit the coexistence of closely related Daphnia clones in the variable and often unpredictable lake environment.

The influence of developmental noise exposure on the temporal processing of acoustical signals in the auditory cortex of rats

Previous experiments have acknowledged that inappropriate or missing auditory inputs during the critical period of development cause permanent changes of the structure and function of the auditory system (Bures et al., 2017). We explore in this study how developmental noise exposure influences the coding of temporally structured stimuli in the neurons of the primary auditory cortex (AC) in Long Evans rats. The animals were exposed on postnatal day 14 (P14) for 12 minutes to a loud (125 dB SPL) broad-band noise. The responses to an amplitude-modulated (AM) noise, frequency-modulated (FM) tones, and click trains, were recorded from the right AC of rats of two age groups: young-adult (ca. 6 months old) and adult (ca. 2 years old), both in the exposed animals and in control unexposed rats. The neonatal exposure resulted in a higher synchronization ability (phase-locking) of the AC neurons for all three stimuli; furthermore, the similarity of neuronal response patterns to repetitive stimulation was higher in the exposed rats. On the other hand, the exposed animals showed a steeper decline of modulation-transfer functions towards higher modulation frequencies/repetition rates. Differences between the two age groups were also apparent; in general, aging had qualitatively the same effect as the developmental exposure. The current results demonstrate that brief noise exposure during the maturation of the auditory system influences both the temporal and the rate coding of periodically modulated sounds in the AC of rats; the changes are permanent and observable up to late adulthood.

Is There More to Within-plant Variation in Seed Size than Developmental Noise?

Within-plant variation in seed size may merely reflect developmental instability, or it may be adaptive in facilitating diversifying bet-hedging, that is, production of phenotypically diverse offspring when future environments are unpredictable. To test the latter hypothesis, we analyzed patterns of variation in seed size in 11 populations of the perennial vine Dalechampia scandens grown in a common greenhouse environment. We tested whether population differences in the mean and variation of seed size covaried with environmental predictability at two different timescales. We also tested whether within-plant variation in seed size was correlated with independent measures of floral developmental instability and increased under stressful conditions. Populations differed genetically in the amount of seed-size variation occurring among plants, among infructescences within plants, and among seeds within infructescences. Within-individual variation was not detectably correlated with measures of developmental instability and did not increase under stress, but it increased weakly with short-term environmental unpredictability of precipitation at the source-population site. These results support the hypothesis that greater variation in seed size is adaptive when environmental predictability is low.

Nature, Nurture, and Noise: Developmental Instability, Fluctuating Asymmetry, and the Causes of Phenotypic Variation

Phenotypic variation arises from genetic and environmental variation, as well as random aspects of development. The genetic (nature) and environmental (nurture) components of this variation have been appreciated since at least 1900. The random developmental component (noise) has taken longer for quantitative geneticists to appreciate. Here, I sketch the historical development of the concepts of random developmental noise and developmental instability, and its quantification via fluctuating asymmetry. The unsung pioneers in this story are Hugo DeVries (fluctuating variation, 1909), C. H. Danforth (random variation between monozygotic twins, 1919), and Sewall Wright (random developmental variation in piebald guinea pigs, 1920). The first pioneering study of fluctuating asymmetry, by Sumner and Huestis in 1921, is seldom mentioned, possibly because it failed to connect the observed random asymmetry with random developmental variation. This early work was then synthesized by Boris Astaurov in 1930 and Wilhelm Ludwig in 1932, and then popularized by Drosophila geneticists beginning with Kenneth Mather in 1953. Population phenogeneticists are still trying to understand the origins and behavior of random developmental variation. Some of the developmental noise represents true stochastic behavior of molecules and cells, while some represents deterministic chaos, nonlinear feedback, and symmetry breaking.

SimBit: A high performance, flexible and easy-to-use population genetic simulator.

SimBit is a general purpose, high performance forward-in-time population genetics simulator. SimBit can simulate a wide variety of selection scenarios (any selection and dominance coefficients variation, any epistatic interaction, any spatial and temporal changes of selection scenario, etc.), demographic scenarios (any changes in patch sizes, migration rates, realistic demography dependent on fecundity, hard vs. soft selection, exponential vs. logistic growth, gametic or zygotic dispersion, etc.) and mating systems (cloning and selfing rates, hermaphrodites or males and females). SimBit can also track QTLs (with hyperdimensional phenotypes, explicit fitness landscape, plasticity, developmental noise, etc.). Finally, SimBit can simulate multiple species with their ecological relationships. SimBit comes with a R wrapper that simplifies the management of an entire research project from the creation of a grid of parameters and corresponding inputs, running simulations and gathering outputs for analysis. SimBit's performance was extensively benchmarked in comparison to SLiM, Nemo and SFS_CODE, varying population size, recombination rate, mutation rate, and the number of loci. I also reproduced simulations from previous studies, benchmarked QTLs and coalescent tree recording techniques. SimBit was most often the highest performing program with the only notable exception of SLiM outperforming SimBit in scenarios with few loci and low genetic diversity.

Filter feeding, deviations from bilateral symmetry, developmental noise, and heterochrony of hemichordate and cephalochordate gills.

We measured gill slit fluctuating asymmetry (FA), a measure of developmental noise, in adults of three invertebrate deuterostomes with different feeding modes: the cephalochordate Branchiostoma floridae (an obligate filter feeder), the enteropneusts Protoglossus graveolens (a facultative filter feeder/deposit feeder) and Saccoglossus bromophenolosus (a deposit feeder). FA was substantially and significantly low in B. floridae and P. graveolens and high in S. bromophenolosus. Our results suggest that the gills of species that have experienced a relaxation of the filter feeding trait exhibit elevated FA. We found that the timing of development of the secondary collagenous gill bars, compared to the primary gill bars, was highly variable in P. graveolens but not the other two species, demonstrating an independence of gill FA from gill bar heterochrony. We also discovered the occasional ectopic expression of a second set of paired gills posterior to the first set of gills in the enteropneusts and that these were more common in S. bromophenolosus. Moreover, our finding that gill slits in enteropneusts exhibit bilateral symmetry suggests that the left‐sidedness of larval cephalochordate gills, and the directional asymmetry of Cambrian stylophoran echinoderm fossil gills, evolved independently from a bilaterally symmetrical ancestor.

Fluctuating Asymmetry, Developmental Noise and Developmental Stability: Future Prospects for the Population Developmental Biology Approach

Developmental noise—which level may vary within a certain backlash allowed by natural selection—is a reflection of the state of a developing system or developmental stability. Phenotypic variations inside the genetically determined norm observed in case of fluctuating asymmetry provide a unique opportunity for evaluating this form of ontogenetic variability. Low levels of developmental noise for the biologic system under study is observed under certain conditions, while its increase acts as a measure of stress. The concordance of changes in developmental stability with changes in other parameters of developmental homeostasis indicates the significance of fluctuating asymmetry estimates. All this determines the future prospects of the study of fluctuating asymmetry not only for developmental biology, but also for population biology. The study of developmental stability may act as the basis of an approach of population developmental biology to assess the nature of the phenotypic diversity and the state of natural populations under various impacts and during evolutionary transformations.