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Inverse Lansing effect: maternal age and provisioning affecting daughters’ longevity and male offspring production

Cora E. Anderson, Camille Homa, Rachael A Jonas-Closs, Leonid Peshkin, Marc W. Kirschner, View ORCID ProfileLev Y. Yampolsky
doi: https://doi.org/10.1101/2021.06.05.447219
Cora E. Anderson
1Department of Biological Sciences, East Tennessee State University, Johnson City TN 37614, USA
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Camille Homa
2Department of Systems Biology, Blavatnik Institute, Harvard Medical School, Boston MA 02115, USA
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Rachael A Jonas-Closs
2Department of Systems Biology, Blavatnik Institute, Harvard Medical School, Boston MA 02115, USA
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Leonid Peshkin
2Department of Systems Biology, Blavatnik Institute, Harvard Medical School, Boston MA 02115, USA
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Marc W. Kirschner
2Department of Systems Biology, Blavatnik Institute, Harvard Medical School, Boston MA 02115, USA
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Lev Y. Yampolsky
1Department of Biological Sciences, East Tennessee State University, Johnson City TN 37614, USA
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  • ORCID record for Lev Y. Yampolsky
  • For correspondence: yampolsk@etsu.edu
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Abstract

Maternal age effects on life history of offspring has been demonstrated in a variety of organisms, more often than not offspring of older mothers having lower life expectancy (Lansing effect). However, there is no consensus on how general this phenomenon is and what are the genetic and epigenetic mechanisms behind it. We tested the predictions of Lansing effect in several Daphnia magna clones in and observed a significant genotype-by-maternal age interaction, indicating clone-specific magnitude and direction of the effect of maternal age on daughters’ longevity. We then repeated this experiment with more detailed life-history and offspring provisioning data focusing on 2 clones with contrasting life-histories. One of these clones demonstrating the inverse Lansing effect, with daughters of older mothers living longer than those of young mothers. Individuals from a single-generation maternal age reversal treatment showed intermediate lifespan. We also report genotype-specific, ambidirectional, and largely fecundity-independent effects of maternal age on daughters’ propensity to produce male offspring, with daughters of older mothers showing higher male production than daughters of younger mothers in the least male-producing clone and vise versa. We tested whether both effects can be explained by either lipid provisioning of embryos by mothers of different age, or by properties of mitochondria transmitted by mothers of different age to their offspring, using rhodamine-123 assay of mitochondrial membrane potential as a measure of mitochondria quality. We show that once lipid provisioning is accounted for, the effects of maternal age on lifespan and male production disappear and that the effect of lipid provisioning itself is clone-dependent, confirming that maternal provisioning sets daughters life history parameters. In the clone showing the inverse Lansing effect we demonstrated that, contrary to the predictions, neonates produced by older mothers were characterized by higher mitochondrial membrane potential in neural tissues than their counterparts born to younger mothers. We conclude that, in at least some genotypes, a reverse Lansing effect is possible, and hypothesize that it may be a result of lower lipid provisioning creating calorically restricted environment during embryonic development.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 07, 2021.
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Inverse Lansing effect: maternal age and provisioning affecting daughters’ longevity and male offspring production
Cora E. Anderson, Camille Homa, Rachael A Jonas-Closs, Leonid Peshkin, Marc W. Kirschner, Lev Y. Yampolsky
bioRxiv 2021.06.05.447219; doi: https://doi.org/10.1101/2021.06.05.447219
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Inverse Lansing effect: maternal age and provisioning affecting daughters’ longevity and male offspring production
Cora E. Anderson, Camille Homa, Rachael A Jonas-Closs, Leonid Peshkin, Marc W. Kirschner, Lev Y. Yampolsky
bioRxiv 2021.06.05.447219; doi: https://doi.org/10.1101/2021.06.05.447219

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