Gene expression in the phenotypically plastic Arctic charr (Salvelinus alpinus): A focus on growth and ossification at early stages of development

Abstract

Gene expression during development shapes the phenotypes of individuals. Although embryonic gene expression can have lasting effects on developmental trajectories, few studies consider the role of maternal effects, such as egg size, on gene expression. Using qPCR, we characterize relative expression of 14 growth and/or skeletal promoting genes across embryonic development in Arctic charr (Salvelinus alpinus). We test to what extent their relative expression is correlated with egg size and size at early life-stages within the study population. We predict smaller individuals to have higher expression of growth and skeletal promoting genes, due to less maternal resources (i.e., yolk) and prioritization of energy toward ossification. We found expression levels to vary across developmental stages and only three genes (Mmp9, Star, and Sgk1) correlated with individual size at a given developmental stage. Contrary to our hypothesis, expression of Mmp9 and Star showed a non-linear relationship with size (at post fertilization and hatching, respectively), whilst Sgk1 was higher in larger embryos at hatching. Interestingly, these genes are also associated with craniofacial divergence of Arctic charr morphs. Our results indicate that early life-stage variation in gene expression, concomitant to maternal effects, can influence developmental plasticity and potentially the evolution of resource polymorphism in fishes.

Figure 1

Relative gene expression correlations with egg/individual size at post fertilization (PF), eye stage (E), hatching (H) and first feeding (FF) in Arctic charr (Salvelinus alpinus) from lake Vatnshlíðarvatn. Note that at PF, two genes (Star and Ets2) were not detected by qPCR and have been removed from the figure. Both linear and non‐linear fits were tested initially for each gene (see Methods section) and the results of the best fitting model represented here. Genes that are significantly correlated with size are Mmp9 at PF, and Sgk1 and Star at H (which best fitted non‐linear, linear and non‐linear models, respectively, see Table S4). Significance levels are indicated in the gene names of the plots by: p *< 0.01, ** < 0.001 and *** < 0.0001. Symbols correspond to different female identities (i.e., different clutches)

Figure 2

Least square (LS) means ± S.E. of relative mRNA expression at four developmental stages: post fertilization (PF), eye stage (E), hatching (H) and first feeding (FF) in Arctic charr (Salvelinus alpinus) from lake Vatnshlíðarvatn. All LS means are significantly different from zero, with the exception of Star and Ets2 at PF stage (not expressed). Least‐square means sharing a letter are not significantly different from each other (Tukey‐adjusted pairwise comparisons of LS means). Above the centerline are growth related genes, and below are genes involved in skeletogenesis