The survival rate of fruit fly embryos was found to depend on the dietary composition of the father prior to mating, report biologists from the University of Cincinnati in collaboration with the University of Western Australia and University of Sydney.
Both macronutrient content and caloric density of the male diet independently affected the likelihood of fruit fly embryos’ survival, the researchers discovered. Additionally, they found more pronounced, and differing, effects on second mating.
“We demonstrate that macronutrient balance and caloric restriction exert significant effects, and that nutritional effects are more impactful when a prior mating has occurred,” wrote lead author Professor Michael Polak.
“Once-mated males produced embryos with marginally elevated mortality under high-caloric densities and a 1: 8 protein: carbohydrate (P: C) ratio. In contrast, embryos produced by twice-mated males were significantly more likely to die under male caloric restriction,” he explained.
"We were really surprised," Polak said. "In many species, the moms do a lot of the care. So we expect there to be an effect from maternal diet on offspring because of that strong link. But it was a real surprise to find a link between paternal diet and offspring."
The outcome may have been due to changes in sperm and seminal fluid quality and composition, and/ or epigenetic paternal effects, speculated the researchers.
Diet also significantly affected the body nutrient reserves of the male fruit flies, thus altering their body condition, which was, in turn, inversely correlated to embryo mortality, the scientists observed.
Female fruit flies were fed identical diets of yeasted cornmeal, whereas 30 different diets were prepared for the male fruit flies. The male diets varied in P: C ratio, caloric density and the sugar type (sucrose or fructose) in the carbohydrate component.
After 17 days on the diets, male flies mated with two females, with a 15-minute interval between each. The scientists counted the eggs after 24 hours and assessed them a further day later to determine how many had hatched or contained viable embryos.
The study results support the theory that dietary effects on the metabolic status of males may influence post-fertilisation outcomes and early developmental processes in offspring, the researchers suggested.
“This link may have implications for understanding the consequences of suboptimal diet for ejaculate quality and reproductive fitness in animals generally,” they explained
The pronounced effect of diet and body condition on embryo survival from the second mating would also point to a possible change in seminal fluid composition because “these results are consistent with patterns of seminal fluid depletion across successive matings,” the researchers observed.
Previous research in fruit flies and other species has shown that depletion of male seminal fluid occurs over successive copulations. Thus, seminal fluid may be involved within protection of the embryo.
"The seminal fluid does have a protective role to play for the embryo. You definitely have implications for embryo health and viability,” commented Polak.
Finally, the researchers speculated that the findings might help to explain female mate choice, on the basis that male appearance in terms of body condition may in fact be a predictor of improved embryo viability.
“Female mate choice on the basis of ornamentation may be selected as a function of a previously underappreciated and relatively ‘cryptic’ direct benefit in the form of a paternally driven influence on embryo viability,” they hypothesised.
Source: Proceedings of the Royal Society B
Published online 11 October 2017 DOI: 10.1098/rspb.2017.1492
“Nutritional geometry of paternal effects on embryo mortality”
Authors: Michal Polak, Leigh W. Simmons, Joshua B. Benoit, Kari Ruohonen, Stephen J. Simpson, Samantha M. Solon-Biet