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Paternal starvation affects metabolic gene expression during zebrafish offspring development and life-long fitness

View ORCID ProfileAda Jimenez-Gonzalez, View ORCID ProfileFederico Ansaloni, Constance Nebendahl, Ghazal Alavioon, David Murray, Weronika Robak, View ORCID ProfileRemo Sanges, View ORCID ProfileFerenc Müller, View ORCID ProfileSimone Immler
doi: https://doi.org/10.1101/2023.09.22.557632
Ada Jimenez-Gonzalez
1Institute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Vincent Drive, Edgbaston, B15 2TT, Birmingham, UK
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Federico Ansaloni
1Institute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Vincent Drive, Edgbaston, B15 2TT, Birmingham, UK
3Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT), Genova, Italy
4Area of Neuroscience, Scuola Internazionale Superiore di Studi Avanzati (SISSA), Trieste, Italy
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Constance Nebendahl
2Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden,
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Ghazal Alavioon
2Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden,
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David Murray
5School of Biological Sciences, University of East Anglia, Norwich, United Kingdom
6Centre for Environment, Fisheries, and Aquaculture Science, Pakefield Road, Lowestoft, NR33 0HT, UK
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Weronika Robak
5School of Biological Sciences, University of East Anglia, Norwich, United Kingdom
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Remo Sanges
3Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT), Genova, Italy
4Area of Neuroscience, Scuola Internazionale Superiore di Studi Avanzati (SISSA), Trieste, Italy
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Ferenc Müller
1Institute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Vincent Drive, Edgbaston, B15 2TT, Birmingham, UK
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  • For correspondence: s.immler@uea.ac.uk f.mueller@bham.ac.uk
Simone Immler
2Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden,
5School of Biological Sciences, University of East Anglia, Norwich, United Kingdom
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  • For correspondence: s.immler@uea.ac.uk f.mueller@bham.ac.uk
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Abstract

Dietary restriction is a putative key to a healthier and longer life, but these benefits may come at a trade-off with reproductive fitness and may affect the following generation(s). The potential inter- and transgenerational effects of starvation are particularly poorly understood in vertebrates when they originate from the paternal line. We utilised the externally fertilising zebrafish amenable to a split-egg clutch design to explore the male-specific effects of starvation on fertility and fitness of offspring independently of maternal contribution. Eighteen days of fasting resulted in reduced fertility in exposed males. While average offspring survival was not affected, we detected higher larval growth in offspring from starved males and increased malformation rates at 24 hours post fertilisation in the F2 embryos produced by the offspring of the starved males. The transcriptome analysis of embryos from starved and fed fathers revealed robust and reproducible induction of muscle composition genes and a contrasting repressive effect on lipid metabolism and lysosome genes. A large proportion of these genes showed enrichment in the yolk syncytial layer suggesting gene regulatory responses associated with metabolism of nutrients through paternal impact on extra embryonic tissues which are loaded with maternally deposited factors. We compared the embryo transcriptome to adult transcriptome datasets and demonstrated comparable repressive effects on metabolism-associated genes. These similarities suggest a physiologically relevant, directed and potentially adaptive response transmitted by the father, independently from the offspring’s nutritional state, which was defined by the mother.

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 4.0 International license.
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Posted September 22, 2023.
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Paternal starvation affects metabolic gene expression during zebrafish offspring development and life-long fitness
Ada Jimenez-Gonzalez, Federico Ansaloni, Constance Nebendahl, Ghazal Alavioon, David Murray, Weronika Robak, Remo Sanges, Ferenc Müller, Simone Immler
bioRxiv 2023.09.22.557632; doi: https://doi.org/10.1101/2023.09.22.557632
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Paternal starvation affects metabolic gene expression during zebrafish offspring development and life-long fitness
Ada Jimenez-Gonzalez, Federico Ansaloni, Constance Nebendahl, Ghazal Alavioon, David Murray, Weronika Robak, Remo Sanges, Ferenc Müller, Simone Immler
bioRxiv 2023.09.22.557632; doi: https://doi.org/10.1101/2023.09.22.557632

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