The conquest of fresh water by the palaemonid shrimps: An evolutionary history scripted in the osmoregulatory epithelia of the gills and antennal glands

Abstract

Extant Palaemonidae occupy aquatic environments that have generated physiological diversity during their evolutionary history. We analyze ultrastructural traits in gills and antennal glands of palaemonid species from distinct osmotic niches, and employ phylogenetic comparative methods to ascertain whether transformations in their osmoregulatory epithelia have evolved in tandem, driven by salinity. Gill pillar cells exhibit apical evaginations whose surface density (Sv, μm2 plasma membrane area/μm3 cytoplasmic volume) ranges from 6.3-7.1 in Palaemon, and 0.7-38.4 in Macrobrachium. In the septal cells, Sv varies from 8.9-10.0 in Palaemon, and 3.3-21.6 in Macrobrachium; mitochondrial volumes (Vmit) range from 43.3-46.8% in Palaemon and 34.9-53.4% in Macrobrachium. In the renal proximal tubule cells, apical microvilli Sv varies from 27.0-34.3 in Palaemon, and 38.3-47.8 in Macrobrachium; basal invagination Sv ranges from 18.7-20.0 in Palaemon and 30.8-40.8 in Macrobrachium. Septal cell Sv shows phylogenetic signal; evagination height/density, apical Sv, and Vmit vary independently of species relatedness. Salt transport capability by the gill and renal epithelia has increased during palaemonid evolution, reflecting amplified membrane availability for ion transporter insertion. These traits underpin the increased osmotic gradients maintained against the external media. Gill ultrastructure and osmotic gradient have evolved in tandem, driven by salinity at the genus level.