As in mammals, seahorse embryos develop internally but, unlike in mammals, this process occurs within a paternal structure (the brood pouch). Functionally, the brood pouch supports developing embryos through placenta-like interactions, but as egg quality is determined by the female's diet, the seahorse system offers opportunities to study the effect of the male's diet on embryo development while varying the female's diet independently. In this study, we investigated the hypothesis that development of seahorse embryos is affected differentially by independent manipulation of the male and female parental diets. Adult males and females were fed separately with either wild-caught crustaceans (Male-W or Female-W, respectively) or commercial aquarium diet (Male-C or Female-C, respectively) for 1 month before conception and during the subsequent pregnancy (approximately 15 days). Dietary unsaturated fatty acid content (18:3n-3) and (20:4n-6) in the W diet was approximately double that in the C diet. In total, 5231 first-brood offspring were obtained from 4 treatment groups formed from (1) Male-W × Female-W; (2) Male-C × Female-W; (3) Male-W × Female-C; and (4) Male-C × Female-C. Each treatment was replicated with 4 couples. Newborns (10 from each brood) were weighed and dimensions measured. Fifteen-day postnatal survival rates were determined from 40 offspring/couple (N at Day 0 = 160/treatment) and fatty acid profiles were evaluated. Data were analysed by nested analyses of covariance (ANCOVA); replicates were nested within treatments and individual offspring measurements were nested within replicates (male and female parental sizes were used as covariates). Offspring produced by the Male-C × Female-W were ~10% taller (both as standard length and tail length; P < 0.05) than those produced by Male-W × Female-W couples but their 15-day survival was poorer (12.9% v. 39%; χ2 = 39.19, 1 DF; P < 0.001). Fifteen-day survival of the other groups was 0% in both cases. When both male and female parents were fed the commercial diet, their offspring were considerably smaller than those from all the other treatments (P < 0.05). The offspring produced by Male-W × Female-C couples showed distortion of the snout:head length ratio, a phenotypic feature that was highly consistent in the Male-W × Female-W treatment group. Fatty acid profiles of the offspring showed significant dependence on the preconception dietary treatment; 20:4n-6 and 22:6n-3 contents were significantly lower in Male-C × Female-C than in Male-W × Female-C (P < 0.01) offspring, showing that the male's pouch could compensate for the poorer quality of lipids derived directly from eggs. These results support the hypothesis that diet received during the preconception period and pregnancy by the males and females differentially affects embryonic growth and fatty acid content, and suggest that seahorses are a suitable model species for understanding the effects of parental diet on offspring health.
Supported by the EU FP7/2007–2013 AquaExcel network (grant agreement No. 262336) and the COST Action (FA1201) (Epigenetics and Periconception Environment).
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