Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage
Abstract Background 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. Result...
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| Format: | Article |
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BMC
2024-02-01
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| Series: | BMC Ecology and Evolution |
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| Online Access: | https://doi.org/10.1186/s12862-024-02203-8 |
| _version_ | 1797276123745222656 |
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| author | Atsuko Sato Yukie Mihirogi Christine Wood Yutaka Suzuki Manuela Truebano John Bishop |
| author_facet | Atsuko Sato Yukie Mihirogi Christine Wood Yutaka Suzuki Manuela Truebano John Bishop |
| author_sort | Atsuko Sato |
| collection | DOAJ |
| description | Abstract Background 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. Results 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. Conclusions 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. |
| first_indexed | 2024-03-07T15:23:48Z |
| format | Article |
| id | doaj.art-592020a586124ee3a763dd24f871c8a6 |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-03-07T15:23:48Z |
| publishDate | 2024-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj.art-592020a586124ee3a763dd24f871c8a62024-03-05T17:25:55ZengBMCBMC Ecology and Evolution2730-71822024-02-0124111410.1186/s12862-024-02203-8Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stageAtsuko Sato0Yukie Mihirogi1Christine Wood2Yutaka Suzuki3Manuela Truebano4John Bishop5Department of Biology, Ochanomizu UniversityDepartment of Biology, Ochanomizu UniversityMarine Biological Association of the UK, The LaboratoryGraduate School of Frontier Sciences, University of TokyoMarine Biology and Ecology Research Center, School of Biological and Marine Sciences, Plymouth UniversityMarine Biological Association of the UK, The LaboratoryAbstract Background 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. Results 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. Conclusions 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.https://doi.org/10.1186/s12862-024-02203-8Sibling speciesHybridHeat stressVariationBet-hedgingSingle-egg sequencing |
| spellingShingle | Atsuko Sato Yukie Mihirogi Christine Wood Yutaka Suzuki Manuela Truebano John Bishop Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage BMC Ecology and Evolution Sibling species Hybrid Heat stress Variation Bet-hedging Single-egg sequencing |
| title | Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage |
| title_full | Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage |
| title_fullStr | Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage |
| title_full_unstemmed | Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage |
| title_short | Heterogeneity in maternal mRNAs within clutches of eggs in response to thermal stress during the embryonic stage |
| title_sort | heterogeneity in maternal mrnas within clutches of eggs in response to thermal stress during the embryonic stage |
| topic | Sibling species Hybrid Heat stress Variation Bet-hedging Single-egg sequencing |
| url | https://doi.org/10.1186/s12862-024-02203-8 |
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