Developmental Instability Research Articles

A Pre-registered Meta-analysis Based on Three Empirical Studies Reveals No Association Between Prenatal (Amniotic) Cortisol Exposure and Fluctuating Asymmetry in Human Infants

Developmental instability (DI) reflects an organism’s inability to develop an ideal phenotype when challenged by genetic and environmental insults. DI can be estimated via the proxy measure of fluctuating asymmetry (FA), i.e., the small random deviations from perfect bilateral symmetry observed in the morphology of paired traits. The mechanisms involved in the genesis of FA in human populations are relatively unknown, though animal research indicates that hormonal processes may be involved. As maternal stress during pregnancy is detrimental to various developmental processes, elevated prenatal cortisol may represent a causal factor in the subsequent emergence of an asymmetrical phenotype. The main purpose of this pre-registered meta-analysis based on three empirical studies was to investigate whether mid-trimester amniotic cortisol levels predict subsequent FA in finger lengths of infants from Germany, Portugal, and the UK. No statistically significant relationships were observed, and meta-analytic combination of the effect size estimates yielded a null result. We did, however, detect significant positive correlations between the cortisol present in the amniotic fluid and maternal plasma in the Portuguese cohort, and observed that FA in the German cohort was significantly lower at 70-months than at either 9- or 20-months. Taken together, the current findings run contrary to animal research showing that elevated prenatal corticosterone exposure leads to increased FA. However, this may be because a single cortisol assay obtained via amniocentesis is an inadequate proxy for average gestational exposure, and/or that prenatal cortisol levels at an earlier (i.e., first rather than second trimester) stage of pregnancy is what explains variance in subsequent FA.

Correction to 'Extreme developmental instability associated with wing plasticity in pea aphids'.

Correction to 'Extreme developmental instability associated with wing plasticity in pea aphids'.

Mandible morphology as a tool to investigate origin, adaptation and stress in invasive alien species: first insights into Callosciurus erythraeus (Rodentia: Sciuridae) in Europe

When an alien species is introduced in a new area, the new population may be genetically and phenotypically different from the parent population because of the population bottleneck, increased inbreeding rate and adaptation to the new environment. In this study we investigated the variation in shape and size of the mandible among and within three populations of the invasive Pallas’s squirrel introduced in Italy, Belgium and France. Significant differences in both size and shape of the mandible were found among all population pairs, with France being the most distinct. French squirrels showed a larger and slenderer mandible with a broad angular process, a restricted condyle, and a backward-oriented coronoid process. The Italian and the Belgian population also differed significantly but to a lesser extent, the Italian squirrels having a lower coronoid process, a broader angular apophysis, and a restricted condyle. Size explained 15% of the total shape variation, but the slope of allometric trajectories did not reveal any significant difference among populations. A significantly high fluctuating and directional asymmetries were found respectively in the French and the Italian squirrels. Results are discussed in terms of different selective pressures in the invaded areas and possible effects of developmental instability.

Fluctuating Asymmetry and Developmental Instability, a Guide to Best Practice

Best practices in studies of developmental instability, as measured by fluctuating asymmetry, have developed over the past 60 years. Unfortunately, they are haphazardly applied in many of the papers submitted for review. Most often, research designs suffer from lack of randomization, inadequate replication, poor attention to size scaling, lack of attention to measurement error, and unrecognized mixtures of additive and multiplicative errors. Here, I summarize a set of best practices, especially in studies that examine the effects of environmental stress on fluctuating asymmetry.

Sensitivity of genital and somatic traits of scorpions to developmental instability caused by increasing urbanization: A 20-year experiment

Urbanization causes the loss of large amounts of habitat and produces significant changes in environmental conditions with consequences in the individual’s behavior, morphology, and physiology in natural populations. The urbanization can impact in the individual’s development instability (DI) that may be measured with the fluctuating asymmetry (FA) level making it an environmental quality bioindicator. In addition, the FA of each trait should be interpreted considering the trait functional importance, morphogenesis and history of selection pressures. In this paper, we evaluated the impact of two decades of increasing urbanization levels over a population of the pampean scorpion Bothriurus bonariensis. We analyze the FA level in somatic and genital traits in adult individuals of both sexes, collected every ~ 10 years (1997, 2008, 2018). Interestingly, in this study the somatic traits (pedipalp chelae) would be under directional selection and are shaped throughout the individual’s growth. In contrast, the genital traits (male’s hemispermatophore) are involved in the sperm transfer process and could be under stabilizing selection. Also, hemispermatophores are affected for less time by environmental stressors since they are formed once the individual has reached sexual maturity. Our results showed a significant increase in the FA levels in somatic traits of males and females, according to the increase of urbanization along years. In contrast, genital traits showed no changes in the level of FA in females, and only a few male genital traits presented an increase in the FA level. This work shows evidence that the measured scorpion traits (under different selective pressures and morphogenesis) might present differences in their susceptibility to environmental stress. We discuss these results in a context of DI of individuals caused by urbanization. We support the idea that the level of FA can be useful as an index to evaluate the effects of environmental stress on invertebrate populations. Furthermore, our paper presents the scorpions as a good model that could be used as an indicator group for studying the impact of the anthropogenic disturbance factors on natural ecosystems.

Modulation of Yorkie activity by alternative splicing is required for developmental stability.

The Hippo signaling pathway is a major regulator of organ growth, which controls the activity of the transcription coactivator Yorkie (Yki) in Drosophila and its homolog YAP in mammals. Both Yki and YAP proteins exist as alternatively spliced isoforms containing either one or two WW domains. The biological importance of this conserved alternative splicing event is unknown. Here, we identify the splicing factor B52 as a regulator of yki alternative splicing in Drosophila and show that B52 modulates growth in part through modulation of yki alternative splicing. Yki isoforms differ by their transcriptional activity as well as their ability to bind and bridge PPxY motifs-containing partners, and can compete in vivo. Strikingly, flies in which yki alternative splicing has been abrogated, thus expressing only Yki2 isoform, exhibit fluctuating wing asymmetry, a signal of developmental instability. Our results identify yki alternative splicing as a new level of modulation of the Hippo pathway, that is required for growth equilibration during development. This study provides the first demonstration that the process of alternative splicing contributes to developmental robustness.

Weak genetic signal for phenotypic integration implicates developmental processes as major regulators of trait covariation.

Phenotypic integration is an important metric that describes the degree of covariation among traits in a population, and is hypothesized to arise due to selection for shared functional processes. Our ability to identify the genetic and/or developmental underpinnings of integration is marred by temporally overlapping cell-, tissue- and structure-level processes that serve to continually 'overwrite' the structure of covariation among traits through ontogeny. Here, we examine whether traits that are integrated at the phenotypic level also exhibit a shared genetic basis (e.g. pleiotropy). We micro-CT scanned two hard tissue traits, and two soft tissue traits (mandible, pectoral girdle, atrium and ventricle, respectively) from an F5 hybrid population of Lake Malawi cichlids, and used geometric morphometrics to extract 3D shape information from each trait. Given the large degree of asymmetric variation that may reflect developmental instability, we separated symmetric from asymmetric components of shape variation. We then performed quantitative trait loci (QTL) analysis to determine the degree of genetic overlap between shapes. While we found ubiquitous associations among traits at the phenotypic level, except for a handful of notable exceptions, our QTL analysis revealed few overlapping genetic regions. Taken together, this indicates developmental interactions can play a large role in determining the degree of phenotypic integration among traits, and likely obfuscate the genotype to phenotype map, limiting our ability to gain a comprehensive picture of the genetic contributors responsible for phenotypic divergence.

Plasticity via feedback reduces the cost of developmental instability.

Costs of plasticity are thought to have important physiological and evolutionary consequences. A commonly predicted cost to plasticity is that plastic genotypes are likely to suffer from developmental instability. Adaptive plasticity requires that the developing organism can in some way sense what environment it is in or how well it is performing in that environment. These two information pathways—an “environmental signal” or a “performance signal” that indicates how well a developing phenotype matches the optimum in the current environment—can differ in their consequences for the organism and its evolution. Here, we consider how developmental instability might emerge as a side‐effect of these two distinct mechanisms. Because a performance cue allows a regulatory feedback loop connecting a trait to a feedback signal, we hypothesized that plastic genotypes using a performance signal would be more developmentally robust compared to those using a purely environmental signal. Using a numerical model of a network of gene interactions, we show that plasticity comes at a cost of developmental instability when the plastic response is mediated via an environmental signal, but not when it is mediated via a performance signal. We also show that a performance signal mechanism can evolve even in a constant environment, leading to genotypes preadapted for plasticity to novel environments even in populations without a history of environmental heterogeneity.

Fluctuating asymmetry of finger lengths, digit ratio (2D:4D), and tattoos: A pre-registered replication and extension of Koziel et al. (2010)

BackgroundTattoos bring risks yet no obvious evolutionary benefit. Koziel et al. (2010) reported increased fluctuating symmetry (a proxy for low developmental instability) in tattooed men, suggesting they could serve as fitness indicators. AimsWe replicate and extend the findings of Koziel et al. by examining fluctuating asymmetry of finger lengths and digit ratio (2D:4D) (a putative indicator of prenatal testosterone exposure) as predictors of adult tattoo prevalence. Study designWe used an online survey with a correlational design. SubjectsParticipants were recruited from the UK and Poland via university participant pools and social media. Data were available for presence/absence of tattoos and at least one predictor variable (composite Fluctuating Asymmetry [cFA], right-hand digit ratio [R2D:4D] and left-hand digit ratio [L2D:4D]) for n = 186 males and n = 997 females. Outcome measuresWe firstly assessed presence/absence of tattoos; when at least one tattoo was present, we also examined overall number and highest visibility. ResultsGreater cFA was associated with lower likelihood of having tattoos in males, though in females greater cFA was associated with higher numbers of tattoos. R2D:4D and L2D:4D correlated negatively with number of tattoos in males, and a positive correlation between L2D:4D and number of tattoos was observed in females. However, these latter findings did not remain significant after controlling for covariates. ConclusionsTattoos may act as fitness indicators in males, though this explanation appears not to extend to females. Prenatal testosterone may also play a role, though doubt is cast on this premise because 2D:4D effects did not remain statistically significant after controlling for covariates.

Breaking Symmetry: Fluctuating Asymmetry and Geometric Morphometrics as Tools for Evaluating Developmental Instability under Diverse Agroecosystems

Fluctuating asymmetry (FA), in contrast with other asymmetries, is the bilateral asymmetry that represents small, random developmental differences between right and left sides. After nearly a century of using traditional morphometrics in the estimation of FA, geometric morphometrics (GM) now provides new insights into the use of FA as a tool, especially for assessing environmental and developmental stress. Thus, it will be possible to assess adaptation to various environmental stressors as particular triggers for unavoidable selection pressures. In this review, we describe measures of FA that use geometric morphometrics, and we include a flow chart of the methodology. We also describe how this combination (GM + FA) has been tested in several agroecosystems. Nutritional stress, temperature, chemical pollution, and population density are known stressors experienced by populations in agroecosystems.

Extreme developmental instability associated with wing plasticity in pea aphids.

A key focus of evolutionary developmental biology is on how phenotypic diversity is generated. In particular, both plasticity and developmental instability contribute to phenotypic variation among genetically identical individuals, but the interactions between the two phenomena and their general fitness impacts are unclear. We discovered a striking example of asymmetry in pea aphids: the presence of wings on one side and the complete or partial absence of wings on the opposite side. We used this asymmetric phenotype to study the connection between plasticity, developmental instability and fitness. We found that this asymmetric wing development (i) occurred equally on both sides and thus is a developmental instability; (ii) is present in some genetically unique lines but not others, and thus has a genetic basis; and (iii) has intermediate levels of fecundity, and thus does not necessarily have negative fitness consequences. We conclude that this dramatic asymmetry may arise from incomplete switching between developmental targets, linking plasticity and developmental instability. We suspect that what we have observed may be a more widespread phenomenon, occurring across species that routinely produce distinct, alternative phenotypes.

Symmetric and Asymmetric Components of Shape Variation in the Diatom Genus Frustulia (Bacillariophyta)

Irregularities in cell division can produce asymmetry in symmetric structures, such as outlines of diatom cells, which can reflect genetic, environmental, or random variability in developmental processes. This study examined 12 phylogenetic lineages of the diatom genus Frustulia using landmark-based geometric morphometrics to assess the variation between cell segments separated by apical and transapical axes. Although asymmetric variation within cells differed in some lineages, these irregularities most likely did not reflect the evolutionary history of the lineages. The intraclonal phenotypic plasticity of diatom frustules was induced rather by nongenetic factors, i.e., inherited valve abnormalities, constraints of siliceous cell walls, and random developmental instability during morphogenesis. The positive correlations between the symmetric and asymmetric components of shape variation indicated that the morphogenesis of diatom cell walls affected irregularities within cells and variability among the symmetrized cells to a similar extent.

Scutation asymmetries in red-footed tortoise Chelonoidis carbonaria Spix, 1824 (Testudines: Testudinidae)

The ability of an individual to withstand random perturbations during its development is considered a good indicator of environmental and genetic stress. A common means of assessing developmental stability is through analysis of fluctuating asymmetry (FA) in bilateral traits. Tortoises, with their large, solid plastron, allow for measurement of body geometry. Their bilateral shell scutes are ideal candidates for asymmetries researches. With this issue in mind we assessed, as a preliminary study, levels of plastron scute asymmetry in a sample of 46 red-footed tortoise Chelonoidis carbonaria from Arauca, N Colombia. We found significative fluctuating asymmetry (FA) but no directional asymmetry, the former not increasing with carapace size and thus indicating that tortoise shells do not become increasingly asymmetrical with age, or in other words, signaling that FA is not being influenced by pholidosis (variability of scale cover mosaic according to the development of the scutes). Asymmetry in plastron shape, although not necessarily apparent at first glance, varied, with gender with males exhibiting higher levels of FA than females. Although we can not identify the potential sources of variation responsible for the observed patterns of developmental instability, we consider this detected form of asymmetry due to unfavorable environmental conditions.

Pace and stability of embryonic development affect telomere dynamics: an experimental study in a precocial bird model.

Prenatal effects on telomere length are increasingly recognized as a potential contributor to the developmental origin of health and adult disease. While it is becoming clear that telomere length is influenced by prenatal conditions, the factors affecting telomere dynamics during embryogenesis remain poorly understood. We manipulated both the pace and stability of embryonic development through varying incubation temperature and its stability in Japanese quail. We investigated the impact on telomere dynamics from embryogenesis to adulthood, together with three potential drivers of telomere shortening, growth rate, oxidative damage and prenatal glucocorticoid levels. Telomere length was not affected by our prenatal manipulation for the first 75% of embryogenesis, but was reduced at hatching in groups experiencing faster (i.e. high temperature) or less stable embryonic development. These early life differences in telomere length persisted until adulthood. The effect of developmental instability on telomere length at hatching was potentially mediated by an increased secretion of glucocorticoid hormones during development. Both the pace and the stability of embryo development appear to be key factors determining telomere length and dynamics into adulthood, with fast and less stable development leading to shorter telomeres, with the potential for adverse associated outcomes in terms of reduced longevity.

Stochastic phenotypic variation: empirical results and potential use in Eurytemora research (Copepoda, Calanoida)

Abstract This study analyses the potential of stochastic phenotypic variation for investigating the population biology of Eurytemora. Stochastic variation is the third component of phenotypic variance, standing on equal footing with genotypic variation and phenotypic plasticity. This is a manifestation of developmental instability and usually increases under stress. In morphological traits, stochastic variation is most often studied using fluctuating asymmetry (FA) of bilateral traits. Here, using data on the FA of nine populations of three Eurytemora species from Europe and North America, we found no correlation between FA and temperature, salinity or tidal amplitude. Invasive American E. carolleeae in the Gulf of Finland (Baltic Sea) had lower FA than the same species in its native Chesapeake Bay, or than E. affinis in its native Gulf of Finland. This pattern may be caused by global warming, which brought Chesapeake Bay temperatures beyond E. carolleeae’s optimal conditions, but made the Gulf of Finland a more suitable environment. Stochastic variation in life history traits is technically more difficult to study, but it may provide important information on fitness. In particular, it manifests in bet-hedging, a risk-spreading strategy beneficial in unpredictable environments. As resting eggs are common in Eurytemora, bet-hedging can be considered a genus strategy. Understanding how stochastic variation contributes to total phenotypic variance may help to interpret changes under unpredictable environmental conditions. Therefore, studies of stochastic phenotypic variation may supply information about the population biology of Eurytemora and other copepods.

Evolution of the Mammalian Ear: An Evolvability Hypothesis

Encapsulated within the temporal bone and comprising the smallest elements of the vertebrate skeleton, the ear is key to multiple senses: balance, posture control, gaze stabilization, and hearing. The transformation of the primary jaw joint into the mammalian ear ossicles is one of the most iconic transitions in vertebrate evolution, but the drivers of this complex evolutionary trajectory are not fully understood. We propose a novel hypothesis: The incorporation of the bones of the primary jaw joint into the middle ear has considerably increased the genetic, regulatory, and developmental complexity of the mammalian ear. This increase in the number of genetic and developmental factors may, in turn, have increased the evolutionary degrees of freedom for independent adaptations of the different functional ear units. The simpler ear anatomy in birds and reptiles may be less susceptible to developmental instabilities and disorders than in mammals but also more constrained in its evolution. Despite the tight spatial entanglement of functional ear components, the increased “evolvability” of the mammalian ear may have contributed to the evolutionary success and adaptive diversification of mammals in the vast diversity of ecological and behavioral niches observable today. A brief literature review revealed supporting evidence for this hypothesis.

Rapid miniaturization of Salvelinus fish as an adaptation to the volcanic impact

Volcanoes serve as natural laboratories expanding our understanding of the recent and past ecological and evolutionary processes. Here, we present data elucidating the developmental and phenotypic transformations providing rapid adaptation for the salmonid fish, Salvelinus malma, to volcanic impact. After being isolated by the mudflow in 1996, the locked descendants of sea-run charr managed to survive in the highly turbid and toxic environment. Initially, the population underwent a phase of high developmental instability accompanied by a surge in morphological deviations. Further, selection targeted the fish prone to migrate into the most toxic mainstream favoring a sedentary lifestyle at the less toxic spawning tributaries. In five–seven generations, the sedentary population recovered developmental homeostasis but diverged into a small-sized short-cycled form with low phenotypic variability. In response to toxicosis, the fish displayed an accelerated metabolic rate and precocious maturations. The spawners possessed fry morphology with no spawning dress. Sedentary fish also exhibited a decreased fecundity and did not build spawning nests. Thus, under the volcanic impact, S. malma demonstrated a rapid paedomorphic miniaturization, an evolutionary mechanism enabling to complete the reproductive cycle under the conditions of high risks of reaching the adaptive capacity limits.

Inbreeding and competition, but not abiotic stresses, increase fluctuating asymmetry ofMimulus guttatusflowers

AbstractGenetic and environmental disturbances are expected to increase developmental instability, which may result in higher fluctuating asymmetry (FA), i.e. small random deviations from symmetry. Plant leaves often do not show this pattern, possibly due to high phenotypic plasticity of leaf shape and low adaptive significance of leaf symmetry. In contrast, symmetry in many animal traits but also in flower shape is considered to be under selection, and FA in such traits may better reflect developmental instability. Using geometric morphometrics, I analysed the symmetry of flowers of inbred and outbred Mimulus guttatus (Phrymaceae) plants grown under five stress treatments with and without grass competition. Flower FA was not increased by abiotic stress, but by inbreeding and competition. As inbreeding and competition affected different principal components of flower FA, different mechanisms may be involved in their effects on FA. FA decreased with individual biomass particularly in selfed offspring, which suggests that inbreeding increased FA particularly when growth was limited by environmental or genetic constraints. Increased flower FA of inbred offspring may explain increased flower handling time and reduced pollinator preference for inbred plants in other M. guttatus studies, and could thus have important consequences for plant demography and plant–pollinator interactions.

Morphometric and morphological analysis of Populus nigra L. leaves in flooded regions

Human activity induced global changes in nature, particularly the flooding regime, which is a stress factor affecting wetland ecosystems. Knowledge of plant strategies of wetland vegetation across a range of flooding gradients is therefore very important. Natural flooding events are increasing as a consequence of constant climate changes. This research was focused on the area of Special Nature Reserve “Gornje Podunavlje” which represents a complex of peculiar marshland, originating from former vast inundated parts of the Danube basin. We have selected samples located on both sides of the embankment in the defended and in the flooded area. The main aim is the assessment of Populus nigra L. riparian tree leaf morphological traits variability (centroid size, shape, developmental instability, specific leaf area and petiole lenght) between two habitats (flooded and not flooded). The geometric morphometry methods were applied to provide visual representation of differences in the leaf shape. We employed leaf composite index indices of fluctuating asymetry as a measure of developmental instability. A statistically ­significant impact of flooding was obtained only for the leaf geometric size and shape, so these traits could be an indicator of flooding as suboptimal environmental conditions.

Divergent scute asymmetry among pure and crossed individuals of Testudo hermanni (Gmelin, 1789)

Fluctuating asymmetry (FA) refers to subtle differences between left and right sides in bilaterally symmetrical organisms or their parts. Both genetic and environmental changes can increase FA, reflecting deterioration in developmental homeostasis of adult morphology due to a loss of developmental stability. In this study, we used geometric morphometric techniques to examine plastral scute asymmetries in a sample of 31 pure and crossed Testudo species (T. hermanni hermanni n = 23 and crosses with T. hermanni boettgeri n = 8) only females by means of 19 anatomical landmarks. Procrustes ANOVA indicated that FA in crossed individuals was significantly higher than that in pure individuals. Crossed individuals also showed a greater degree of phenotypic plasticity than T. hermanni hermanni. We conclude that crosses among T. hermanni hermanni and T. hermanni boettgeri can increase homozygosity and are responsible for greater developmental instabilities. Nonetheless, more information on crossed phenotypes could be of great interest to raise pure Hermann’s tortoises for reintroduction programmes. Key words: Carapace, Geometric morphometrics, Hybridization, Plastron, Testudines