Xia Fanning, Santacruz Ana, Wu Di, Bertho Sylvain, Fritz Elizabeth, Morales-Sosa Pedro, McKinney Sean, Nowotarski Stephanie H, Rohner Nicolas
Stowers Institute for Medical Research, Kansas City, MO, USA.
Stowers Institute for Medical Research, Kansas City, MO, USA.
Dev Biol. 2025 Jul;523:82-98. doi: 10.1016/j.ydbio.2025.04.006. Epub 2025 Apr 11.
Reproduction is a fundamental biological process for the survival and continuity of species. Examining changes in reproductive strategies offers valuable insights into how animals have adapted their life histories to different environments. Since reproduction is one of the most energy-intensive processes in female animals, nutrient scarcity is expected to interfere with the ability to invest in gametes. Lately, a new model to study adaptation to nutrient limitation has emerged; the Mexican tetra Astyanax mexicanus. This fish species exists as two different morphs, a surface river morph and a cave-dwelling morph. The cave-dwelling morph has adapted to the dark, lower biodiversity, and nutrient-limited cave environment and consequently evolved an impressive starvation resistance. However, how reproductive strategies have adapted to nutrient limitations in this species remains poorly understood. Here, we compared breeding activities and maternal contributions between laboratory-raised surface fish and cavefish. We found that cavefish produce different clutch sizes of eggs with larger yolk compared to surface fish, indicating a greater maternal nutrient deposition in cavefish embryos. To systematically characterize yolk compositions, we used untargeted proteomics and lipidomics approaches to analyze protein and lipid profiles in 2-cell stage embryos and found an increased proportion of sphingolipids in cavefish compared to surface fish. Additionally, we generated transcriptomic profiles of surface fish and cavefish ovaries using a combination of single cell and bulk RNA sequencing to examine differences in maternal contribution. We found that genes essential for hormone regulation were upregulated in cavefish follicular somatic cells compared to surface fish. To evaluate whether these differences contribute to their reproductive abilities under natural-occurring stress, we induced breeding in starved female fish. Remarkably, cavefish maintained their ability to breed under starvation, whereas surface fish largely lost this ability. We identified insulin-like growth factor 1a receptor (igf1ra) as a potential candidate gene mediating the downregulation of ovarian development genes, potentially contributing to the starvation-resistant fertility of cavefish. Taken together, we investigated the female reproductive strategies in Astyanax mexicanus, which will provide fundamental insights into the adaptations of animals to environments with extreme nutrient deficit.
繁殖是物种生存和延续的基本生物学过程。研究繁殖策略的变化有助于深入了解动物如何根据不同环境调整其生活史。由于繁殖是雌性动物最耗能的过程之一,营养物质的匮乏预计会影响其对配子的投入能力。最近,一种研究对营养限制适应的新模型出现了,即墨西哥丽脂鲤(Astyanax mexicanus)。这种鱼类存在两种不同的形态,一种是生活在河流表面的形态,另一种是穴居形态。穴居形态的鱼已经适应了黑暗、生物多样性较低且营养有限的洞穴环境,因此进化出了令人印象深刻的抗饥饿能力。然而,该物种的繁殖策略如何适应营养限制仍知之甚少。在这里,我们比较了实验室饲养的河流表面鱼类和穴居鱼类的繁殖活动及母体贡献。我们发现,与河流表面鱼类相比,穴居鱼类产出的卵的卵块大小不同,且卵黄更大,这表明穴居鱼类胚胎中母体营养物质的沉积更多。为了系统地表征卵黄成分,我们使用非靶向蛋白质组学和脂质组学方法分析了2细胞期胚胎中的蛋白质和脂质谱,发现与河流表面鱼类相比,穴居鱼类中鞘脂的比例增加。此外,我们结合单细胞和大量RNA测序生成了河流表面鱼类和穴居鱼类卵巢的转录组图谱,以研究母体贡献的差异。我们发现,与河流表面鱼类相比,穴居鱼类卵泡体细胞中对激素调节至关重要的基因上调。为了评估这些差异是否有助于它们在自然应激下的繁殖能力,我们诱导饥饿的雌鱼进行繁殖。值得注意的是,穴居鱼类在饥饿状态下仍保持繁殖能力,而河流表面鱼类则基本丧失了这种能力。我们确定胰岛素样生长因子1a受体(igf1ra)是介导卵巢发育基因下调的潜在候选基因,这可能有助于穴居鱼类抗饥饿的繁殖能力。综上所述,我们研究了墨西哥丽脂鲤的雌性繁殖策略,这将为动物对极端营养缺乏环境的适应提供基本见解。