Buffered EGFR signaling regulated by spitz to argos expression ratio is critical for patterning the Drosophila eye

The Epidermal Growth Factor Receptor (EGFR) signaling pathway plays a critical role in regulating tissue patterning. Drosophila EGFR (DER) signaling achieves specificity through multiple ligands and feedback loops to finetune signaling spatiotemporally. The principal Drosophila EGF, cleaved Spitz, and the negative feedback molecule, Argos are diffusible and can act both in a cell autonomous and non-autonomous manner. The relative expression dose of Spitz and Argos early in development has been shown to be critical in patterning the Drosophila eye, but the exact identity of the cells expressing these genes in the larval eyedisc has been elusive. Using single molecule RNA Fluorescence in situ Hybridization (smFISH), we reveal an intriguing differential expression of spitz and argos in the Drosophila third instar eye imaginal disc indicative of directional DER signaling. By genetically tuning DER signaling, we show that rather than absolute levels of expression, the ratio of expression to be critical for determining the adult eye phenotype. Proper ommatidial patterning is robust to thresholds around a tightly maintained wildtype ratio, and breaks down beyond. This provides a powerful instance of developmental buffering.

Prolonged exposure to constant environmental conditions prompts nonrandom genetic variation

ABSTRACTLong-term environmental exposure under selection-free conditions has no consequences for fitness under the neo-Darwinian paradigm but it may provoke adaptive developmental buffering if environmental pressures foster directional organismal changes. To test this hypothesis, we revisited a Mutation Accumulation (MA) experiment where isogenic lines of the ciliate Paramecium were propagated for >40 sexual cycles (∼4 years) in a nearly selection-free and nutrient-rich environment. We find that these MA lines’ somatic genome is enriched with intervening segments of DNA (IESs), which are normally eliminated during germline-soma differentiation. Across independent replicate MA lines, an excess of these somatic IESs fall into a class of epigenetically controlled sequences, map to the same genomic locations, and preferentially disrupt loci that regulate nutrient metabolism. Although further work is needed to assess the phenotypic consequences of somatic IESs, these findings support a model where environmentally induced developmental variants may restore an adaptive fit between phenotype and environment. In this model, positive selection is surprisingly dispensable for adaptation.

Modulation and Evolution of Animal Development through microRNA Regulation of Gene Expression

microRNAs regulate gene expression by blocking the translation of mRNAs and/or promoting their degradation. They, therefore, play important roles in gene regulatory networks (GRNs) by modulating the expression levels of specific genes and can tune GRN outputs more broadly as part of feedback loops. These roles for microRNAs provide developmental buffering on one hand but can facilitate evolution of development on the other. Here we review how microRNAs can modulate GRNs during animal development as part of feedback loops and through their individual or combinatorial targeting of multiple different genes in the same network. We then explore how changes in the expression of microRNAs and consequently targets can facilitate changes in GRNs that alter development and lead to phenotypic evolution. The reviewed studies exemplify the key roles played by microRNAs in the regulation and evolution of gene expression during developmental processes in animals.

Chaperones, Canalization, and Evolution of Animal Forms

Over half a century ago, British developmental biologist Conrad Hal Waddington proposed the idea of canalization, that is, homeostasis in development. Since the breakthrough that was made by Rutherford and Lindquist (1998), who proposed a role of Hsp90 in developmental buffering, chaperones have gained much attention in the study of canalization. However, recent studies have revealed that a number of other molecules are also potentially involved in canalization. Here, I introduce the emerging role of DnaJ chaperones in canalization. I also discuss how the expression levels of such buffering molecules can be altered, thereby altering organismal development. Since developmental robustness is maternally inherited in various organisms, I propose that dynamic bet hedging, an increase in within-clutch variation in offspring phenotypes that is caused by unpredictable environmental challenges to the mothers, plays a key role in altering the expression levels of buffering molecules. Investigating dynamic bet hedging at the molecular level and how it impacts upon morphological phenotypes will help our understanding of the molecular mechanisms of canalization and evolutionary processes.

Decanalization of wing development accompanied the evolution of large wings in high-altitude Drosophila

In higher organisms, the phenotypic impacts of potentially harmful or beneficial mutations are often modulated by complex developmental networks. Stabilizing selection may favor the evolution of developmental canalization—that is, robustness despite perturbation—to insulate development against environmental and genetic variability. In contrast, directional selection acts to alter the developmental process, possibly undermining the molecular mechanisms that buffer a trait’s development, but this scenario has not been shown in nature. Here, we examined the developmental consequences of size increase in highland Ethiopian Drosophila melanogaster. Ethiopian inbred strains exhibited much higher frequencies of wing abnormalities than lowland populations, consistent with an elevated susceptibility to the genetic perturbation of inbreeding. We then used mutagenesis to test whether Ethiopian wing development is, indeed, decanalized. Ethiopian strains were far more susceptible to this genetic disruption of development, yielding 26 times more novel wing abnormalities than lowland strains in F2 males. Wing size and developmental perturbability cosegregated in the offspring of between-population crosses, suggesting that genes conferring size differences had undermined developmental buffering mechanisms. Our findings represent the first observation, to our knowledge, of morphological evolution associated with decanalization in the same tissue, underscoring the sensitivity of development to adaptive change.

Phenotypic variation of the housefly, Musca domestica: amounts and patterns of wing shape asymmetry in wild populations and laboratory colonies

Musca domestica L. (Diptera: Muscidae) is a vector of a range variety of pathogens infecting humans and animals. During a year, housefly experiences serial population bottlenecks resulted in reduction of genetic diversity. Population structure has also been subjected to different selection regimes created by insect control programs and pest management. Both environmental and genetic disturbances can affect developmental stability, which is often reflected in morphological traits as asymmetry. Since developmental stability is of great adaptive importance, the aim of this study was to examine fluctuating asymmetry (FA), as a measure of developmental instability, in both wild populations and laboratory colonies of M. domestica. The amount and pattern of wing shape FA was compared among samples within each of two groups (laboratory and wild) and between groups. Firstly, the amount of FA does not differ significantly among samples within the group and neither does it differ between groups. Regarding the mean shape of FA, contrary to non-significant difference within the wild population group and among some colonies, the significant difference between groups was found. These results suggest that the laboratory colonies and wild samples differ in buffering mechanisms to perturbations during development. Hence, inbreeding and stochastic processes, mechanisms dominating in the laboratory-bred samples contributed to significant changes in FA of wing shape. Secondly, general patterns of left–right displacements of landmarks across both studied sample groups are consistent. Observed consistent direction of FA implies high degrees of wing integration. Thus, our findings shed light on developmental buffering processes important for population persistence in the environmental change and genetic stress influence on M. domestica.