Maternal Experience with Predation Risk Influences Genome-Wide Embryonic Gene Expression in Threespined Sticklebacks (<i>Gasterosteus aculeatus</i>)

<div><p>There is growing evidence for nongenetic effects of maternal experience on offspring. For example, previous studies have shown that female threespined stickleback fish (<i>Gasterosteus aculeatus</i>) exposed to predation risk produce offspring with altered behavior, metabolism and stress physiology. Here, we investigate the effect of maternal exposure to predation risk on the embryonic transcriptome in sticklebacks. Using RNA-sequencing we compared genome-wide transcription in three day post-fertilization embryos of predator-exposed and control mothers. There were hundreds of differentially expressed transcripts between embryos of predator-exposed mothers and embryos of control mothers including several non-coding RNAs. Gene Ontology analysis revealed biological pathways involved in metabolism, epigenetic inheritance, and neural proliferation and differentiation that differed between treatments. Interestingly, predation risk is associated with an accelerated life history in many vertebrates, and several of the genes and biological pathways that were identified in this study suggest that maternal exposure to predation risk accelerates the timing of embryonic development. Consistent with this hypothesis, embryos of predator-exposed mothers were larger than embryos of control mothers. These findings point to some of the molecular mechanisms that might underlie maternal effects.</p></div

Exposing mothers to a predator led to an overall activation of genes in stickleback embryos.

<p>The heatmap shows the general pattern of gene regulation for the 295 genes differentially expressed (EdgeR) as a result of maternal exposure to predation risk. Red  =  upregulated, blue  =  downregulated compared to the mean value of a gene from all samples. Rows represent genes and columns represent clutches (one clutch per mother, n = 16 mothers total). log(CPM) data are normalized for library size and scaled so that every gene has the same mean (0) and standard deviation; units of change are standard deviations from the mean, and each row has the same range of color values.</p

The most overrepresented biological functions (n≥10 molecules) from an enrichment analysis (Ingenuity Pathway Analysis software) of genes differentially expressed as a result of maternal exposure to predation risk.

<p># molecules  =  the number of unique RNA molecules (i.e. differentially expressed genes) associated with a function within the IPA database; p-value  =  the enrichment p-value for the function; Sample molecules  =  a sample of genes associated with the function that were differentially expressed in maternally-stressed embryos compared to embryos of control mothers in the direction of regulation expected for association with the biological function.</p

Maternal exposure to predation risk altered expression of embryonic genes involved in neural growth and epigenetic modification.

<p>A) The expression of DNA methyltransferase genes, histone genes, and genes that interact with histone and DNA methylation in 3dpf stickleback embryos from mothers exposed to a predator and control mothers. B) The expression of genes involved in the proliferation and differentiation of neurons. Each bar represents the mean ± standard error of the logarithm of adjusted Counts Per Million mapped reads across clutches of embryos from n = 8 mothers, and 10 pooled embryos per clutch. NS = raw p-value>0.05, *p<0.05, **p<0.01, ***p<0.001.</p

The most overrepresented biological annotations from the list of genes differentially expressed as a result of maternal exposure to predation risk.

<p>Genes were mapped to their associated biological process (BP_FAT), cellular component (CC_FAT), molecular function (MF_FAT), and KEGG pathways using <i>Homo sapiens</i> gene annotations and genome background within the DAVID Functional Annotation Tool (v6.7). Only terms with FDR <0.05 and ≥2 genes were included.</p

Fundulus notatus raw data

Excel file containing the raw data (morphometric measurements as well as data on population, drainage, habitat, age, and sex)