Fasting increases investment in soma upon refeeding at the cost of gamete quality in zebrafish

Ivimey‐Cook, Edward; Murray, David S.; Coriolis, Jean-Charles de; Edden, Nathan; Immler, Simone; Maklakov, Alexei A.

doi:10.1098/rspb.2022.1556

Cited by 3 publications

(1 citation statement)

References 58 publications

(76 reference statements)

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“…The integrity of germ cells is important, and their maintenance may come at the expense of somatic maintenance (Chen et al., 2020; Ivimey‐Cook et al., 2023). This link between somatic health and reproductive fitness may help explain our findings of faster growth but reduced reproductive fitness in F1 offspring from starved males.…”

Section: Discussionmentioning

confidence: 99%

Paternal starvation affects metabolic gene expression during zebrafish offspring development and lifelong fitness

Jimenez‐Gonzalez,

Ansaloni,

Nebendahl

et al. 2024

Molecular Ecology

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Dietary restriction in the form of fasting 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 long‐term fasting and 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 fasting/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 increased larval growth rate in F1 offspring from starved males and more malformed embryos at 24 h post‐fertilisation in F2 offspring produced by F1 offspring from starved males. Comparing the transcriptomes of F1 embryos sired by starved and fed fathers revealed robust and reproducible increased expression of muscle composition genes but lower expression of lipid metabolism and lysosome genes in embryos from starved fathers. A large proportion of these genes showed enrichment in the yolk syncytial layer suggesting gene regulatory responses associated with metabolism of nutrients through paternal effects on extra‐embryonic tissues which are loaded with maternal factors. We compared the embryo transcriptomes to published adult transcriptome datasets and found comparable repressive effects of starvation 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.

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Section: Discussionmentioning

confidence: 99%

Paternal starvation affects metabolic gene expression during zebrafish offspring development and lifelong fitness

Jimenez‐Gonzalez,

Ansaloni,

Nebendahl

et al. 2024

Molecular Ecology

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The evolution of ageing: classic theories and emerging ideas

Mc Auley

2024

Biogerontology

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Ageing is generally regarded as a non-adaptive by-product of evolution. Based on this premise three classic evolutionary theories of ageing have been proposed. These theories have dominated the literature for several decades. Despite their individual nuances, the common thread which unites them is that they posit that ageing results from a decline in the intensity of natural selection with chronological age. Empirical evidence has been identified which supports each theory. However, a consensus remains to be fully established as to which theory best accounts for the evolution of ageing. A consequence of this uncertainty are counter arguments which advocate for alternative theoretical frameworks, such as those which propose an adaptive origin for ageing, senescence, or death. Given this backdrop, this review has several aims. Firstly, to briefly discuss the classic evolutionary theories. Secondly, to evaluate how evolutionary forces beyond a monotonic decrease in natural selection can affect the evolution of ageing. Thirdly, to examine alternatives to the classic theories. Finally, to introduce a pluralistic interpretation of the evolution of ageing. The basis of this pluralistic theoretical framework is the recognition that certain evolutionary ideas will be more appropriate depending on the organism, its ecological context, and its life history.

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Fasting increases investment in soma upon refeeding at the cost of gamete quality in zebrafish

et al. 2023

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Fasting increases lifespan in invertebrates, improves biomarkers of health in vertebrates and is increasingly proposed as a promising route to improve human health. Nevertheless, little is known about how fasted animals use resources upon refeeding, and how such decisions affect putative trade-offs between somatic growth and repair, reproduction and gamete quality. Such fasting-induced trade-offs are based on strong theoretical foundations and have been recently discovered in invertebrates, but the data on vertebrates are lacking. Here, we report that fasted female zebrafish, Danio rerio , increase investment in soma upon refeeding, but it comes at a cost of egg quality. Specifically, an increase in fin regrowth was accompanied by a reduction in 24 h post-fertilization offspring survival. Refed males showed a reduction in sperm velocity and impaired 24 h post-fertilization offspring survival. These findings underscore the necessity of considering the impact on reproduction when assessing evolutionary and biomedical implications of lifespan-extending treatments in females and males and call for careful evaluation of the effects of intermittent fasting on fertilization.

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Fasting increases investment in soma upon refeeding at the cost of gamete quality in zebrafish

Cited by 3 publications

References 58 publications

Paternal starvation affects metabolic gene expression during zebrafish offspring development and lifelong fitness

Paternal starvation affects metabolic gene expression during zebrafish offspring development and lifelong fitness

The evolution of ageing: classic theories and emerging ideas

Fasting increases investment in soma upon refeeding at the cost of gamete quality in zebrafish

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