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 taken to the extreme by the Syngnathidae, in which male pregnancy is one of the most astonishing idiosyncrasies. However, critical and timedependent environmental effects on developing embryos, such as those extensively studied in mammalian pregnancy, have not been investigated in the male pregnancy context. Here, we tested the hypothesis that seahorse pregnancy is subject to 'critical windows' of environmental sensitivity by feeding male long-snouted seahorses (Hippocampus reidi) a diet deficient in polyunsaturated fatty acids during specific periods before and during pregnancy. Despite embryos being nourished principally by maternally supplied yolk, we found that offspring morphology, fatty acid composition and gene expression profiles were influenced by paternal diet in a manner that depended critically on the timing of manipulation. Specifically, reception of a diet deficient in polyunsaturated fatty acids in the days preceding pregnancy resulted in smaller newborn offspring, while the same diet administered towards the end of pregnancy resulted in substantial alterations to newborn gene expression and elongation of the snout at 10 days old. Although paternal diet did not affect 10 day survival, the observed morphological alterations in some cases could have important fitness consequences in the face of natural selective pressures such as predation and food availability. Our results demonstrate that, under male pregnancy, fine-scale temporal variation in parental diet quality and subsequent critical window effects should not be overlooked as determinants of developing offspring fitness.

A Multidisciplinary Experimental Study on the Effects of Breeders Diet on Newborn Seahorses (Hippocampus guttulatus)

“…Hence, the initial quality of eggs/newborn could be improved by feeding the breeders on a high quality diet for at least 3 months in advance of the onset of the breeding season, which is in agreement with previous findings in the tropical species H. reidi (Planas and Chamorro, 2019). That finding is of primary importance to female diets as it is noteworthy that embryos are mostly dependent on maternal nutrition (yolk quality) until later stages of development, when the embryos are mostly dependent on paternal contribution (Otero-Ferrer et al, 2020).…”

“…Fry quality can be manipulated to a certain extend by modifying the nutritional composition of the diet during the breeding season of fishes (Fernández-Palacios et al, 2011) including seahorses (Otero-Ferrer et al, 2020). However, it is also important to assess the effect of preconception diet on reproduction success and the contribution of males and females, as reported by in H. hippocampus.…”

A comparative analysis of the ontogeny of syngnathids (pipefishes & seahorses) reveals how heterochrony contributed to their diversification

“…Therefore, N. ophidion presents itself as an indirect developing species with a pronounced larval stage, while the development of S. typhle and H. erectus is much more direct, possibly as a result or by-product of their more derived form of male pregnancy. 5,6,13 Thus, developmental stage upon release may be linked to the lineage (with Nerophinae featuring a larval stage and Syngnathinae not), pregnancy type (with Nerophis likely not providing nutrients to embryos, while this is more likely/shown for (some) Syngnathinae 51,52 ), or other factors not considered here and /or their interactions.…”

Pre-breeding Diets in the Seahorse Hippocampus reidi: How Do They Affect Fatty Acid Profiles, Energetic Status and Histological Features in Newborn?

“…However, the effect of enhanced diets provided to H. kuda females on egg size was limited to the first spawning (Saavedra et al, 2014). From a nutritional and energetical point of view, the roles played by seahorse males and females in the production of eggs and neonates remain unclear, even though the contribution of males (and the effect of their diets) seems to be important in nutritional supply (Skalkos et al, 2020) and a key determinant in newborn quality (Otero-Ferrer et al, 2020).…”

“…A singular characteristic of seahorses is reproduction, in which females provide most nutrients to eggs whereas males take care and also supply nutrients to embryos developing from eggs transferred by females to their brood pouches (Carcupino et al, 2002;Skalkos et al, 2020;Wittington and Friesen, 2020). Mating and parturition are highly synchronized with egg maturation so that the release of eggs and newborn occur almost simultaneously and at similar time intervals, which vary depending on species, temperature, and breeder's diet (Lin et al, 2006(Lin et al, , 2007Planas et al, 2010;Otero-Ferrer et al, 2020). In seahorses, the assessment of nutritional and energetic requirements in seahorse breeders is lacking.…”