RNA sequencing of early round goby embryos reveals that maternal experiences can shape the maternal RNA contribution in a wild vertebrate

Abstract

Background: It has been proposed that non-genetic inheritance could promote species fitness. Non-genetic inheritance could allow offspring to benefit from the experience of their parents, and could advocate pre-adaptation to prevailing and potentially selective conditions. Indeed, adaptive parental effects have been modeled and observed, but the molecular mechanisms behind them are far from understood.

Results: In the present study, we investigated whether maternal RNA can carry information about environmental conditions experienced by the mother in a wild vertebrate. Maternal RNA directs the development of the early embryo in many non-mammalian vertebrates and invertebrates. However, it is not known whether vertebrate maternal RNA integrates information about the parental environment. We sequenced the maternal RNA contribution from a model that we expected to rely on parental effects: the invasive benthic fish species Neogobius melanostomus (Round Goby). We found that maternal RNA expression levels correlated with the water temperature experienced by the mother before oviposition, and identified temperature-responsive gene groups such as core nucleosome components or the microtubule cytoskeleton.

Conclusions: Our findings suggest that the maternal RNA contribution may incorporate environmental information. Maternal RNA should therefore be considered a potentially relevant pathway for non-genetic inheritance. Also, the ability of a species to integrate environmental information in the maternal RNA contribution could potentially contribute to species fitness and may also play a role in extraordinary adaptive success stories of invasive species such as the round goby.

Keywords: Neogobius melanostomus; maternal contribution; non-genetic inheritance; parental effects; short term adaptation.

Fig. 1

Sampling, sequencing and verification of the Neogobius melanostomus maternal RNA contribution. a, Visualization of embryonic development by actin staining. 2-cell, 8-cell, > 32-cell, and organogenesis stage are depicted. Scale bar: 1 mm. See Additional file 1: Figure S1 for a full panel of developmental stages. b, Sampling. The ascending line represents water temperature at the sampling site. Dashed lines and dots indicate sampling dates and samples, respectively. The temperature curve during five days before each sampling date is colored orange. c, Developmental stage of sequenced samples in relation to the mean water temperature during five days before oviposition. Each dot represents a sample. d, The round goby orthologs of maternally contributed genes in the zebrafish [49] are highly expressed in pre-MZT N. melanostomus embryos

Fig. 2

The expression of maternally contributed RNAs correlates with maternally experienced mean, maximum, and minimum temperature, but not with control parameters. a, Density plot of the Spearman correlation coefficients calculated between expression level and indicated parameters. b, Barplot showing the number of open reading frames that correlate with mean temperature experienced by the mother before oviposition (green) or with cleavage stage (black) at the indicated correlation values

Fig. 3

The maternal temperature experience before oviposition has a global effect on the maternal RNA contribution. a, Variance explained by individual principal components. b, PC1 correlates with the mean temperature experienced by the mother. c, PC1 and PC2 together explain mean temperature experienced by the mother. d, Cleavage progress, genetic dissimilarity, or temperature interval experienced by the mother are independent from PC1 and PC2

Fig. 4

Functional analysis of the temperature response. a, Correlation analysis and PCA identify overlapping sets of genes. b, Open reading frames which react to higher temperature with increased expression are more conserved. c, Pathways and functions of temperature sensitive maternal genes, manual annotation. Dot size corresponds to the number of genes with that function. d, GO term clusters identified among temperature sensitive maternal genes by the DAVID annotation tool. Dot size corresponds to DAVID enrichment score