Surviving on limited resources: effects of caloric restriction on growth, gene expression and gut microbiota in a species with male pregnancy (Hippocampus erectus)

Abstract

The positive health effects of caloric restriction (CR) have been widely studied in a few conventional model species, displaying typically conventional reproductive roles, with females investing more in parental care. This creates a bias in the current literature about the impact of CR between males and females in species with unconventional reproductive strategies. In this study, we investigated the effects of CR on growth, gene expression, and intestinal microbiota in the lined seahorseHippocampus erectus.Juvenile seahorses were subjected to ad libitum (AL) or every other day fasting for 5 months. Total mRNA sequencing of liver, head kidney and gonad tissue, along with 16SrRNA amplicon sequencing of hind intestine samples was done to investigate sex-adverse effects of fasting in a species with male pregnancy and thus distinct life-history strategies leading to sex-specific trade-offs in resource allocation. Our results indicate that fasting caused a general stunting effect and delayed brood pouch development in males, reflecting its energetic demands and possibly delaying reproduction till more resources are available. We found both organ and sex-specific gene expression responses to CR, with liver and ovaries displaying the strongest variation. In the liver of CR female seahorses, numerous genes linked to energy and lipid synthesis were upregulated, and in the ovaries of the same, we found downregulation of inflammatory markers. These results reflect the fasted female’s need to allocate more resources to eggs to increase reproductive chances earlier in life compared to males. There was no sex-specific response to CR in the microbiota, rather both fasted males and females displayed similar higher alpha-diversity and increased abundance of Proteobacteria and Bacteroidetes compared to AL fed seahorses. Our research suggests that male and female reactions to nutrient scarcity may depend on their resource allocation to reproduction and parental investment, rather than directly on their biological sex. Our findings highlight the importance of using species displaying a broader range of reproductive strategies, sex role, mating system and life-history strategies when studying the sex-specific effects of CR.