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

Abstract

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.

Keywords: dietary restriction; fasting; gamete; soma; trade-off; zebrafish.

Figure 1.

Sex-specific caudal fin regrowth prior to refeeding (a) and after refeeding (b). Colours represent fasted (blue, dashed lines) or fed (red, solid lines) dietary treatments in females (left) or males (right). Lines, points and 95% CIs represent predicted values from a linear model.

Figure 2.

(a,c) Age-specific reproduction. Colours represent fasted (blue, dashed lines) or fed (red, solid lines) dietary treatments in females (left) or males (right). Lines, points and 95% CIs represent predicted values from a linear model. (b,d) Total number of offspring in either female (left, red) or males (right, blue). Lines, points and 95% CIs represent predicted values from a linear model. (a,b) Reproduction whilst individuals are within their respective dietary treatments. (c,d) Reproduction when all individuals have been placed back into ad libitum.

Figure 3.

Age-specific egg survival during (a) or post-fasting (b). Colours represent fasted (blue, dashed lines) or fed (red, solid lines) dietary treatments in females (left) or males (right). Lines, points and 95% CIs represent predicted values from a linear model.

Figure 4.

(a) Age-specific sperm curvilinear velocity (VCL) or (b) average path velocity (VAP) during (left) or post-fasting (right). Colours represent fasted (blue, dashed lines) or fed (red, solid lines) dietary treatments in males. Lines, points and 95% CIs represent predicted values from a linear model.

Figure 5.

(a) Parental sex-specific fry growth between days 3 and 5 post-fertilization. Colours represent fasted (blue, dashed lines) or fed (red, solid lines) dietary treatments in female (left) or male parents (right). (b) Hourly fry growth in either female (left, red) or male parents (right, blue). Lines, points and 95% CIs represent predicted values from a linear model.

Figure 6.

Proposed allocation decisions of females (yellow) and males (orange) after fasting when organisms resume full-feeding. We note that, for males, offspring traits are measured using a control female. Females trade offspring quality for offspring number and somatic maintenance. Males trade offspring number and quality for somatic maintenance. The orange or yellow filled circle denotes where the trade-off was observed during this experiment.