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Cytosine methylation patterns suggest a role of methylation in plastic and adaptive responses to temperature in European grayling (Thymallus thymallus) populations.

ABSTRACT: Temperature is a key environmental parameter affecting both the phenotypes and distributions of organisms, particularly ectotherms. Rapid organismal responses to thermal environmental changes have been described for several ectotherms; however, the underlying molecular mechanisms often remain unclear. Here, we studied whole genome cytosine methylation patterns of European grayling (Thymallus thymallus) embryos from five populations with contemporary adaptations of early life history traits at either 'colder' or 'warmer' spawning grounds. We reared fish embryos in a common garden experiment using two temperatures that resembled the 'colder' and 'warmer' conditions of the natal natural environments. Genome-wide methylation patterns were similar in populations originating from colder thermal origin subpopulations, whereas single nucleotide polymorphisms uncovered from the same data identified strong population structure among isolated populations, but limited structure among interconnected populations. This was surprising because the previously studied gene expression response among populations was mostly plastic, and mainly influenced by the developmental temperature. These findings support the hypothesis of the magnified role of epigenetic mechanisms in modulating plasticity. The abundance of consistently changing methylation loci between two warmer-to-colder thermal origin population pairs suggests that local adaptation has shaped the observed methylation patterns. The dynamic nature of the methylomes was further highlighted by genome-wide and site-specific plastic responses. Our findings support both the presence of a plastic response in a subset of CpG loci, and the evolutionary role of methylation divergence between populations adapting to contrasting thermal environments.

SUBMITTER: Savilammi T

PROVIDER: S-EPMC7901546 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe structure and diversity of grayling (Thymallus thymallus) populations have been well studied in most of its native habitat; however the southernmost populations of the Balkan Peninsula remain largely unexplored. The purpose of this study was to assess the genetic diversity of Serbian grayling populations, detect the impact of stocking and provide guidelines for conservation and management.MethodsEighty grayling individuals were collected from four rivers (Ibar, Lim, Drina and Rzav). The mitochondrial DNA control region (CR; 595 bp of the 3'end and 74 bp of flanking tRNA) and the ATP6 gene (630 bp fragment) were sequenced for 20 individuals (five from each locality). In addition, all individuals were genotyped with 12 microsatellite loci. The diversity and structure of the populations as well as the recent and ancient population declines were studied using specialized software.ResultsWe detected three new haplotypes in the mtDNA CR and four haplotypes in the ATP6 gene of which three had not been described before. Previously, one CR haplotype and two ATP6 gene haplotypes had been identified as allochthonous, originating from Slovenia. Reconstruction of phylogenetic relations placed the remaining two CR haplotypes from the River Danube drainage of Serbia into a new clade, which is related to the previously described sister Slovenian clade. These two clades form a new Balkan clade. Microsatellite marker analysis showed that all four populations are genetically distinct from each other without any sign of intra-population structure, although stocking of the most diverse population (Drina River) was confirmed by mtDNA analysis. Recent and historical population declines of Serbian grayling do not differ from those of other European populations.ConclusionsOur study shows that (1) the Ibar, Lim and Drina Rivers grayling populations are genetically distinct from populations outside of Serbia and thus should be managed as native populations in spite of some introgression in the Drina River population and (2) the Rzav River population is not appropriate for further stocking activities since it originates from stocked Slovenian grayling. However, the Rzav River population does not represent an immediate danger to other populations because it is physically isolated from these.

Project description:We studied a Norwegian metapopulation of grayling, a spring-spawning freshwater salmonid fish with high homing propensity that has undergone contemporary evolution of early life-history in response to temperature. Samples derived from four spawning sites in four grayling sub-populations in Lake Lesjaskogsvatnet (62 14'N 8 25'E) in southern Norway. Adult grayling were captured at the four spawning sites, stripped of gametes and fertilized eggs were reared in two temperature treatments in common garden conditions as to represent lower and upper temperatures experienced by developing grayling larvae in nature. Proteins were isolated using a standard sodium dodecyl sulphate (SDS)-based extraction method. For trypsin digestion and peptide-level iTRAQ labeling, samples were peptide-labeled with isobaric tags by iTRAQ reagents (4-plex, Applied Biosystems) following the manufacturer's instructions. To clean and fractionate each sample we employed an isotope coded affinity tag procedure (ICAT) using the ICAT Cation Exchange Buffer Pack - Cation Exchange Cartridge system (Applied Biosystems). Four peptide fractions were collected using four concentrations of the elution buffer (50 mM, 100 mM, 150 mM, and 350 mM KH2PO4). Peptides were desalted using C18 macrospin columns (The Nest Group, Southborough, MA). For LC-MS/MS, peptides were separated by reversed-phase chromatography using an Easy-nLC II nanoflow system connected to an Orbitrap Velos mass spectrometer (Thermo Fisher Scientific, Bremen, Germany). Peptides were separated at a flow rate of 300 nl/min with 102 min gradients as follows: initially 2 % B to 25% B (60 min), 40% B (90 min), and 100% B (92-102 min). Protein identification and quantification were done using the ProteinPilotTM v.4 program (Applied Biosystems). In the parameters we selected the Paragon method, iodoacetamide for cys alkylation, trypsin for digestion, thorough ID for search effort, biological modifications and amino acid substitutions for ID focus, and bias correction in quantification. As a search database we used all Atlantic salmon (Salmo salar) submitted in the UniProt database (www.uniprot.org) up to March 2012. To evaluate the accuracy of the quantification method, we also did a pilot experiment. We spiked the six-protein mix provided with the iTRAQ kit in ratios 1:3:10 in samples that contained an equal amount of protein extract from a grayling embryo. Then we labeled each sample with a different isobaric tag (114:115:116, respectively). The aim was to employ the proposed methodology to quantify a subset of proteins that change across samples in a cloud of background proteins that remain unchanged and these data are also provided in the dataset.

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Cytosine methylation patterns suggest a role of methylation in plastic and adaptive responses to temperature in European grayling (Thymallus thymallus) populations.

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