Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage

TL;DR

This study explores how thermal stress during embryonic development affects the diversity of maternal mRNAs in eggs across generations.

Contribution

The study introduces a novel model system and experimental approach to investigate how maternal thermal stress influences developmental heterogeneity in egg mRNA provisioning.

Findings

Maternal thermal stress reduces heterogeneity in maternal mRNA provision in the eggs of the stressed individual.

The next generation shows increased heterogeneity in egg mRNA provisioning despite being unstressed.

Signaling molecule expression heterogeneity is directly affected by thermal stress, unlike developmental buffering genes.

Abstract

The origin of variation is of central interest in evolutionary biology. Maternal mRNAs govern early embryogenesis in many animal species, and we investigated the possibility that heterogeneity in maternal mRNA provisioning of eggs can be modulated by environmental stimuli.

We employed two sibling species of the ascidian Ciona, called here types A and B, that are adapted to different temperature regimes and can be hybridized. Previous study showed that hybrids using type B eggs had higher susceptibility to thermal stress than hybrids using type A eggs. We conducted transcriptome analyses of multiple single eggs from crosses using eggs of the different species to compare the effects of maternal thermal stress on heterogeneity in egg provisioning, and followed the effects across generations. We found overall decreases of heterogeneity of egg maternal mRNAs associated with maternal thermal stress. When the eggs produced by the F1 AB generation were crossed with type B sperm and the progeny (‘ABB’ generation) reared unstressed until maturation, the overall heterogeneity of the eggs produced was greater in a clutch from an individual with a heat-stressed mother compared to one from a non-heat-stressed mother. By examining individual genes, we found no consistent overall effect of thermal stress on heterogeneity of expression in genes involved in developmental buffering. In contrast, heterogeneity of expression in signaling molecules was directly affected by thermal stress.

Due to the absence of batch replicates and variation in the number of reads obtained, our conclusions are very limited. However, contrary to the predictions of bet-hedging, the results suggest that maternal thermal stress at the embryo stage is associated with reduced heterogeneity of maternal mRNA provision in the eggs subsequently produced by the stressed individual, but there is then a large increase in heterogeneity in eggs of the next generation, although itself unstressed. Despite its limitations, our study presents a proof of concept, identifying a model system, experimental approach and analytical techniques capable of providing a significant advance in understanding the impact of maternal environment on developmental heterogeneity.

The online version contains supplementary material available at 10.1186/s12862-024-02203-8.

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