Time-critical influences of gestational diet in a seahorse model of male pregnancy

Abstract

Sex role reversal is not uncommon in the animal kingdom but is takento the extreme by the Syngnathidae, in which male pregnancy is oneof the most astonishing idiosyncrasies. However, critical and timedependentenvironmental effects on developing embryos, such asthose extensively studied in mammalian pregnancy, have not beeninvestigated in the male pregnancy context. Here, we tested thehypothesis that seahorse pregnancy is subject to 'critical windows' ofenvironmental sensitivity by feeding male long-snouted seahorses(Hippocampus reidi) a diet deficient in polyunsaturated fatty acidsduring specific periods before and during pregnancy. Despiteembryos being nourished principally by maternally supplied yolk,we found that offspring morphology, fatty acid composition and geneexpression profiles were influenced by paternal diet in a manner thatdepended critically on the timing of manipulation. Specifically,reception of a diet deficient in polyunsaturated fatty acids in thedays preceding pregnancy resulted in smaller newborn offspring,while the same diet administered towards the end of pregnancyresulted in substantial alterations to newborn gene expression andelongation of the snout at 10 days old. Although paternal diet did notaffect 10 day survival, the observed morphological alterations in somecases could have important fitness consequences in the face ofnatural selective pressures such as predation and food availability.Our results demonstrate that, under male pregnancy, fine-scaletemporal variation in parental diet quality and subsequent criticalwindow effects should not be overlooked as determinants ofdeveloping offspring fitness.