Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto 14040-901, SP, Brazil.
Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião 11600-000, SP, Brazil.
Integr Comp Biol. 2022 Aug 25;62(2):376-387. doi: 10.1093/icb/icac081.
Early marine invertebrates like the Branchiopoda began their sojourn into dilute media some 500 million years ago in the Middle Cambrian. Others like the Mollusca, Annelida, and many crustacean taxa have followed, accompanying major marine transgressions and regressions, shifting landmasses, orogenies, and glaciations. In adapting to these events and new habitats, such invertebrates acquired novel physiological abilities that attenuate the ion loss and water gain that constitute severe challenges to life in dilute media. Among these taxon-specific adaptations, selected from the subcellular to organismal levels of organization, and constituting a feasible evolutionary blueprint for invading freshwater, are reduced body permeability and surface (S) to volume (V) ratios, lowered osmotic concentrations, increased osmotic gradients, increased surface areas of interface epithelia, relocation of membrane proteins in ion-transporting cells, and augmented transport enzyme abundance, activity, and affinity. We examine these adaptations in taxa that have penetrated into freshwater, revealing diversified modifications, a consequence of distinct body plans, morpho-physiological resources, and occupation routes. Contingent on life history and reproductive strategy, numerous patterns of osmotic regulation have emerged, including intracellular isosmotic regulation in weak hyper-regulators and well-developed anisosmotic extracellular regulation in strong hyper-regulators, likely reflecting inertial adaptations to early life in an estuarine environment. In this review, we address osmoregulation in those freshwater invertebrate lineages that have successfully invaded this biotope. Our analyses show that across 66 freshwater invertebrate species from six phyla/classes that have transmuted into freshwater from the sea, hemolymph osmolalities decrease logarithmically with increasing S:V ratios. The arthropods have the highest osmolalities, from 300 to 650 mOsmoles/kg H2O in the Decapoda with 220-320 mOsmoles/kg H2O in the Insecta; osmolalities in the Annelida range from 150 to 200 mOsmoles/kg H2O, and the Mollusca showing the lowest osmolalities at 40-120 mOsmoles/kg H2O. Overall, osmolalities reach a cut-off at ∼200 mOsmoles/kg H2O, independently of increasing S:V ratio. The ability of species with small S:V ratios to maintain large osmotic gradients is mirrored in their putatively higher Na+/K+-ATPase activities that drive ion uptake processes. Selection pressures on these morpho-physiological characteristics have led to differential osmoregulatory abilities, rendering possible the conquest of freshwater while retaining some tolerance of the ancestral medium.
早期的海洋无脊椎动物，如介形类，大约在 5 亿年前的中寒武纪就开始进入低盐度环境。其他无脊椎动物，如软体动物、环节动物和许多甲壳类动物也随之而来，伴随着海洋的大规模进退、陆地的迁移、造山运动和冰川作用。为了适应这些事件和新的栖息地，这些无脊椎动物获得了新的生理能力，可以减轻构成低盐度环境生存挑战的离子丢失和水分获取。在这些特定于分类群的适应中，从亚细胞到生物体水平的组织选择，并构成了入侵淡水的可行进化蓝图，包括降低的身体通透性和表面积（S）与体积（V）的比率、降低的渗透压浓度、增加的渗透压梯度、增加的界面上皮表面积、离子转运细胞中膜蛋白的重新定位以及增加的转运酶丰度、活性和亲和力。我们检查了已经进入淡水的分类群中的这些适应，揭示了多样化的变化，这是由于不同的体型、形态生理资源和占据途径造成的。根据生活史和生殖策略，出现了许多不同的渗透调节模式，包括弱超调节者的细胞内等渗调节和强超调节者的发达的非等渗细胞外调节，这可能反映了对早期河口环境生活的惯性适应。在这篇综述中，我们研究了那些成功入侵这种生物栖息地的淡水无脊椎动物的渗透压调节。我们的分析表明，在来自六个门/纲的 66 种淡水无脊椎动物中，从海洋转变为淡水的物种，血淋巴渗透压与 S:V 比值呈对数下降。节肢动物的渗透压最高，十足目达 300-650 毫渗摩尔/千克 H2O，昆虫纲为 220-320 毫渗摩尔/千克 H2O；环节动物的渗透压范围为 150-200 毫渗摩尔/千克 H2O，软体动物的渗透压最低，为 40-120 毫渗摩尔/千克 H2O。总的来说，渗透压在大约 200 毫渗摩尔/千克 H2O 处达到一个截止值，与 S:V 比值的增加无关。具有小 S:V 比值的物种维持大渗透压梯度的能力反映在它们推测的更高的 Na+/K+-ATPase 活性上，这种酶活性驱动离子摄取过程。对这些形态生理特征的选择压力导致了不同的渗透压调节能力，使征服淡水成为可能，同时保留了对原始介质的一定耐受性。
