skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Epigenetics and the evolution of form: Experimental manipulation of a chromatin modification causes species‐specific changes to the craniofacial skeleton
Abstract A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype–phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape inMaylandia, but not inTropheops. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time‐ and species‐dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species‐specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation.  more » « less
Award ID(s):
1942178
PAR ID:
10479268
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Evolution & Development
ISSN:
1520-541X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Synopsis Epigenetic mechanisms are increasingly understood to have major impacts across ecology. However, one molecular epigenetic mechanism, DNA methylation, currently dominates the literature. A second mechanism, histone modification, is likely important to ecologically relevant phenotypes and thus warrants investigation, especially because molecular interplay between methylation and histone acetylation can strongly affect gene expression. There are a limited number of histone acetylation studies on non-model organisms, yet those that exist show that it can impact gene expression and phenotypic plasticity. Wild birds provide an excellent system to investigate histone acetylation, as free-living individuals must rapidly adjust to environmental change. Here, we screen histone acetylation in the house sparrow (Passer domesticus); we studied this species because DNA methylation was important in the spread of this bird globally. This species has one of the broadest geographic distributions in the world, and part of this success is related to the way that it uses methylation to regulate its gene expression. Here, we verify that a commercially available assay that was developed for mammals can be used in house sparrows. We detected high variance in histone acetylation among individuals in both liver and spleen tissue. Further, house sparrows with higher epigenetic potential in the Toll Like Receptor-4 (TLR-4) promoter (i.e., CpG content) had higher histone acetylation in liver. Also, there was a negative correlation between histone acetylation in spleen and TLR-4 expression. In addition to validating a method for measuring histone acetylation in wild songbirds, this study also shows that histone acetylation is related to epigenetic potential and gene expression, adding a new study option for ecological epigenetics. 
    more » « less
  2. Histone post-translational modifications (PTMs) are epigenetic marks that operate within the central dogma of molecular biology: upon an environmental stimulus, the histone PTMs surrounding DNA can be changed in a way that modifies gene expression, and, therefore, the abundance and composition of RNA and proteins within cells (1). Once a change is induced, histone PTMs can offer organisms resilience to their environments through processes such as developmental plasticity (2, 3). The purpose of this study was to investigate whether histone PTMs mediate developmental plasticity in Mozambique tilapia facing salinity challenges. To this aim, we exposed fish to either freshwater or hypersalinity during their early critical window of development, then continued to raise the fish in either freshwater or seawater, respectively, for 18 months. Once the fish reached adulthood, we acclimated them to either freshwater or seawater. Following salinity treatments, we quantified 343 histone PTMs in the gills of each fish. We show here that histone PTMs differ dramatically between fish exposed to distinct environmental conditions for 18 months, and that the majority of histone PTM alterations persist for at least four weeks. However, histone PTMs respond minimally to salinity acclimation during adulthood. These results challenge our prior assumptions regarding the timescale of the histone PTM response, demonstrating that it does not necessarily precede the proteomic response or acclimation. Although this finding complicates our interpretation of developmental plasticity, it signifies that histone PTMs reflect prolonged exposure to environmental conditions. 
    more » « less
  3. How complex morphologies evolve is one of the central questions in evolutionary biology. Observing the morphogenetic events that occur during development provides a unique perspective on the origins and diversification of morphological novelty. One can trace the tissue of origin, emergence, and even regression of structures to resolve murky homology relationships between species. Here, we trace the developmental events that shape some of the most diverse organs in the animal kingdom—the male terminalia (genitalia and analia) ofDrosophilids. Male genitalia are known for their rapid evolution with closely related species of theDrosophilagenus demonstrating vast variation in their reproductive morphology. We used confocal microscopy to monitor terminalia development during metamorphosis in twelve related species ofDrosophila. From this comprehensive dataset, we propose a new staging scheme for pupal terminalia development based on shared developmental landmarks, which allows one to align developmental time points between species. We were able to trace the origin of different substructures, find new morphologies and suggest possible homology of certain substructures. Additionally, we demonstrate that posterior lobe is likely originated prior to the split between theDrosophila melanogasterand theDrosophila yakubaclade. Our dataset opens up many new directions of research and provides an entry point for future studies of theDrosophilamale terminalia evolution and development. 
    more » « less
  4. Abstract Culex pipiens, the northern house mosquito, is a major vector of West Nile virus. To survive the severe winter, adult mosquitoes enter a diapause programme. Extended lifespan and an increase in lipid storage are key indicators of diapause. Post‐translational modifications to histone proteins impact the expression of genes and have been linked to the lifespan and energy utilisation of numerous insects. Here, we investigated the potential contribution of epigenetic alterations in initiating diapause in this mosquito species. Multiple sequence alignment of H3 sequences from other insect species demonstrates a high conservation of the H3 histone inCx. pipiensthroughout evolution. We then compared the levels of histone methylation in the ovaries and fat body tissues of diapausing and non‐diapausingCx. pipiensusing western blots. Our data indicate that histone methylation levels in the ovaries ofCx. pipiensdo not change during diapause. In contrast, H3K27me2 levels decrease more than twofold in the fat body of diapausing mosquitoes relative to non‐diapausing counterparts. H3K27 methylation plays a crucial role in chromosome activation and inactivation during development in many insect species. This is predominantly governed by polycomb repressor complex 2. Intriguingly, a previous ChIP‐seq study demonstrated that the transcription factor FOXO (Forkhead box O) targets the genes that comprise this complex. In addition, H3K27me2 exhibits dynamic abundance throughout the diapause programme inCx. pipiens, suggesting its potential role in the initial activation of the diapause programme. This study expands our understanding of the relationship between alterations in epigenetic regulation and diapause. 
    more » « less
  5. null (Ed.)
    Histone post-translational modifications (PTMs) are epigenetic marks that modify the state of chromatin and lead to alterations in gene expression. Advances in mass spectrometry have enabled the high-throughput analysis of histone PTMs without the need for prior knowledge of individual PTMs of interest. In this study, the global histone PTM landscape was analyzed in the gills, kidney, and testes of Mozambique tilapia (Oreochromis mossambicus) through tandem mass spectrometry using data dependent acquisition (DDA-LCMS2) and PTM mapping approaches. PTM assignment to a specific amino acid was validated using A-score and localization probability scores that are based on the detection of diagnostic MSMS ions. These values signify the robustness of PTM assignment to a specific residue within the protein sequence. For PTMs that were represented by both modified and unmodified versions of the corresponding peptide, the stoichiometry was calculated and compared between tissues. We have identified multiple types of histone PTMs and assigned them to specific residues in each tissue. These PTMs include acetylation, methylation, demethylation, trimethylation, phosphorylation/ dehydration, and ubiquitination. Our results indicate that the gills, kidney, and testes each display a unique profile of histone PTMs. These data provide a strong basis for the generation of spectral libraries that enable high-throughput quantitative analyses of histone PTM stoichiometry on a global scale in tilapia exposed to diverse environmental and developmental contexts. 
    more » « less