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Viala, S.

Publications and source records attributed to Viala, S..

8 recordsLinked to original sources

DNA methylation in the water strider Microvelia longipes is driven by genetics, not diet

Phenotypic plasticity, the ability of a single genotype to produce alternative phenotypes in response to environmental cues, is a key driver of evolutionary change. In the water strider Microvelia longipes, males display remarkable continuous variation in hindleg length, a sexually selected trait used as a weapon in male male contests for access to females. To determine whether DNA methylation mediates this environmentally induced phenotypic variation, we used three inbred lines of M. longipes showing differences in mean hindleg length, body size, and allometric coefficients. Whole-genome bisulfite sequencing (WGBS) on adult males and females from all lines determined that about 12% of the 12,684,876 CpG sites found in the genome were methylated. This global level of DNA methylation is among the highest reported in insects. DNA methylation was predominantly concentrated within or near gene bodies (77% of methylated CpGs), consistent with patterns observed in other insects. Unsupervised clustering and principal component analyses revealed that methylation patterns differed significantly between genetic lines but showed minimal differences between sexes, indicating a strong genetic influence. Most surprisingly, nutritional treatment followed by leg-specific WGBS failed to identify any change in DNA methylation despite nutrition having a pronounced effect on leg length. These results show that in M. longipes, DNA methylation patterns are largely stable across nutritional treatments and primarily determined by genetic background. This challenges the common assumption that DNA methylation universally mediates environmentally induced phenotypic plasticity and suggests that other epigenetic mechanisms, such as histone modifications or non-coding RNAs, may play a more direct role in regulating continuous plastic traits. Our study underscores the complexity of epigenetic regulation and highlights the need for broader investigation of molecular pathways to fully understand the molecular basis of phenotypic variation in natural populations.

evolutionary biology↗

Nutrition mediates extreme growth variation through deep changes in gene expression in the water strider Microvelia longipes

Exaggerated sexually selected traits are known to be highly variable and their degree of expression is dependent on nutritional input. Yet the molecular mechanisms linking nutritional variation to phenotypic variation remain poorly understood. Here, we investigate how nutritional input shapes the development of male rear leg length, an exaggerated and highly variable trait in the water strider Microvelia longipes, using comparative transcriptomics and RNA interference gene knockdown experiments. We demonstrate that nutrition is the primary driver of gene expression variation, with male exaggerated rear legs exhibiting the highest number of nutrition-responsive genes. Moreover, the increase in morphological divergence between leg types or sex, which is systematically exacerbated by rich nutrition, is associated with increased number of leg-biased genes. These comparative analyses allowed us to identify BMP11 as specifically enriched in female and male rear legs. Knockdown of BMP11 abolishes nutritional plasticity in leg length only in males, positioning it as a key integrator of environmental, sex and developmental signals. Our findings reveal that transcriptional modulation provides a molecular interface between nutrition and trait exaggeration. This work advances our understanding of how environmental cues are translated into complex phenotypes and highlights the role of developmental plasticity as a substrate for evolutionary change.

evolutionary biology↗

Sexual conflict, directional sexual selection and phenotypic plasticity jointly drive the evolution of extreme phenotypic variation

How broad phenotypic variation is maintained in natural populations in the face of selection is a central question in evolutionary biology. We address this question in the water strider Microvelia longipes, where males exhibit striking variation in rear leg length used in male-male contests for dominance. Using reaction norm experiments on inbred lines, we demonstrate that phenotypic plasticity contributes to expanding phenotypic variation, but requires high genetic variation to generate the broad range of trait expression observed in natural populations. Experimental evolution favouring trait exaggeration revealed that directional sexual selection not only fails to erode variation of male rear leg length, but rather amplifies it beyond the natural distribution. Additionally, male-limited selection in favour of dominance generated substantial fecundity costs in females, underscoring the role of sexual conflict driven by females in constraining exaggerated secondary sexual traits in males. Our findings show that sexually antagonistic selection and directional sexual selection jointly generate high genetic variation, which phenotypic plasticity inflates into broad phenotypic distribution of male weapon size. This provides an empirical explanation for the high variability of male exaggerated weapons in nature.

evolutionary biology↗

Jag2 patterns early differentiation in the epidermal stem cell layer

Adult stem cell function depends on continuous input from the surrounding microenvironment. However, the cues that pattern this function in high turnover tissue that undergo continuous cellular remodeling remain poorly understood. Here we demonstrate that inputs from epithelial neighbors at distinct stages of differentiation cooperatively influence cell fate in the skin epidermis. Stem cells initiate differentiation of their neighbors via the Notch ligand Jag2, linking fate decisions to the composition of the local stem cell environment. When this signal is lost, misoriented divisions and engagement with distinct ligands in the suprabasal layers can partially restore upward flux differentiating cells. Although these mechanisms help to sustain barrier function, they ultimately disrupt tissue architecture, underscoring the need for balanced fates in the stem cell compartment. Together, our findings demonstrate that distinct cellular environments reinforce early epidermal differentiation, with stem cells themselves acting as key mediators of cell fate and tissue organization.

cell biology↗

Engulfing to Adapt: Efferocytosis by Epithelial Cells Triggers Cell State Transitions During Tissue Remodeling

Hormone deprivation treatments are a leading approach in prostate cancer treatment. Following deprivation, the organ regresses from a fully differentiated secretory organ to one less than 50% of the original size, that has been reprogrammed to a state primed for regeneration. Despite widespread use of hormone treatments, the events linking cellular apoptotic responses following prostate hormone deprivation and cell state reprogramming are not fully understood. We report that the absence of hormones creates a microenvironment rich in apoptotic cells that are engulfed by neighboring prostate epithelial cells. Mechanistically, we found that epithelial cells alter their metabolism and gene expression during efferocytosis. Efferocytic epithelial cells adopt a more glycolytic metabolism, resulting in elevated levels of lactate production. This correlates with increased histone Lactylation over gene regulatory elements for genes regulating autophagy and catabolism. To further demonstrate that efferocytosis is necessary to remodel tissue during regression, we expressed a mutant of the receptor protein MFGE8, MFGE8-D89E to "mask" PtdSer in the prostate epithelium and reduce efferocytosis. This effectively prevented the cell and lumen size changes hormone-deprived prostates usually go through. Our findings suggest new perspectives on how epithelial cell efferocytosis can impact tissue remodeling and altered cellular states.

developmental biology↗

Context effects on repair of 5'-overhang DSB induced by Cas12a in Arabidopsis.

Sequence-specific endonucleases have been key to the study of the mechanisms and control of DNA double-strand break (DSB) repair and recombination and the availability of CRISPR-Cas nucleases over the last decade has driven rapid progress in understanding and application of targeted recombination in many organisms, including plants. We present here an analysis of recombination at targeted chromosomal 5overhang DSB generated by the FnCas12a endonuclease in the plant, Arabidopsis thaliana. The much-studied Cas9 nuclease cleaves DNA to generate blunt-ended, double-strand breaks (DSB), but relatively less is known about the repair of other types of breaks, such as those with 5-overhanging ends. Sequencing the repaired breaks clearly shows that the majority of repaired DSB carry small deletions and are thus repaired locally by End-Joining recombination, confirmed by Nanopore sequencing of larger amplicons. Paired DSB generate deletions at one or both cut-sites, as well as deletions and reinsertions of the deleted segment between the two cuts, visible as inversions. While differences are seen in the details, overall the deletion patterns are similar between repair at single-cut and double-cut events, notwithstanding the fact that only the former involve cohesive DNA overhangs. A strikingly different repair pattern is however observed at breaks flanked by direct repeats. This change in sequence context results in the presence of an alternative class of repair events, corresponding to highly efficient repair by Single-strand Annealing recombination.

genetics↗

A single giant cell at the origin of an evolutionary innovation

Key innovations play a central role in the diversification of lineages, yet our understanding of the mechanisms underlying their emergence remains fragmented. The propelling fan is a key innovation associated with the diversification of Rhagovelia water striders into fast flowing streams. Here, we show that a single giant cell is responsible for the development of the fan throughout embryogenesis. RNA interference against the fan-specific gene family gsha/mogsha depleted the fan in the embryo but did not alter the giant cell, indicating that these genes are not required for specifying the identity of this cell. gsha/mogsha instead seem to activate the expression of cuticular genes during early development, suggesting a role of these genes in regulating the accumulation of fan structural proteins. We also show that Hox genes act to block the giant cell in the fore- and rear-legs, thus restricting its fate to the mid-legs - the pair of legs that generates movement on water. In addition, Hox expression is specifically excluded from the giant cell, thus allowing the expression of the fans developmental genetic program. This study reveals that a single cell can be sufficient to generate innovative traits that have been central for a lineage to acquire new ecological opportunities and burst into diversification. One-sentence summaryA single giant cell orchestrates the developmental genetic program of a key innovation

evolutionary biology↗

Transcriptome-based phylogeny of the semi-aquatic bugs (Hemiptera: Heteroptera: Gerromorpha) reveals patterns of lineage expansion in a series of new adaptive zones

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, they have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. The monophyletic group of water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a group of insects that transited to live on the water-air interface and diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones, representing distinct niches of water surfaces, and further diversification of the group. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

evolutionary biology↗