Otero-Ferrer Francisco, Lättekivi Freddy, Ord James, Reimann Ene, Kõks Sulev, Izquierdo Marisol, Holt William Vincent, Fazeli Alireza
Grupo en Biodiversidad y Conservación, Instituto Universitario en Acuicultura Sostenible y Ecosistemas Marinos (IU-ECOAQUA), Universidad de Las Palmas de Gran Canaria, Marine Scientific and Technological Park, Carretera de Taliarte s/n, E-35214 Telde, Spain.
Institute of Biomedicine and Translational Medicine, Department of Pathophysiology, University of Tartu, Ravila 14b, 50411 Tartu, Estonia.
J Exp Biol. 2020 Feb 7;223(Pt 3):jeb210302. doi: 10.1242/jeb.210302.
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 time-dependent 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 () 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.
性别角色逆转在动物王国中并不罕见，但在海龙科中却达到了极致，其中雄性怀孕是最令人惊讶的特性之一。然而，对于发育中的胚胎，诸如在哺乳动物怀孕中广泛研究的那些关键且依赖时间的环境影响，在雄性怀孕的背景下尚未得到研究。在这里，我们通过在怀孕前和怀孕期间的特定时期给雄性长吻海马喂食缺乏多不饱和脂肪酸的食物，来检验海马怀孕受到环境敏感性“关键窗口期”影响这一假设。尽管胚胎主要由母体提供的卵黄滋养，但我们发现后代的形态、脂肪酸组成和基因表达谱受到父本饮食的影响，且这种影响在很大程度上取决于操作的时间。具体而言，在怀孕前几天接受缺乏多不饱和脂肪酸的饮食会导致新生后代体型较小，而在怀孕末期给予相同饮食则会导致新生后代基因表达发生显著变化以及10日龄时吻部变长。尽管父本饮食不影响10日龄时的存活率，但在面对诸如捕食和食物可获得性等自然选择压力时，在某些情况下观察到的形态改变可能会对适应性产生重要影响。我们的结果表明，在雄性怀孕的情况下，亲代饮食质量的细微时间变化以及随后的关键窗口期效应作为发育中后代适应性的决定因素不应被忽视。
