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, μm 2 plasma membrane area/μm 3 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.

Understanding the molecular basis of adaptation to freshwater environments by prawns in the genus Macrobrachium

“…A number of species are also commercially important in culture worldwide, and Macrobrachium species can be found in virtually all water types across the planet . Species in this genus exhibit impressive osmoregulatory capacity (McNamara et al, 2015), and represent a particularly attractive and convenient group for investigating adaptive mechanisms involved with a freshwater lifestyle.…”

“…The major obstacle during freshwater adaptation is to deal with osmotic stress and to restrict ion loss from the body in a dilute medium (McNamara et al, 2015). The crustacean gill is well known to play a principal role in osmoregulation and maintenance of ionic balance while the antennal gland (main excretory organ and used to absorb ions) is also known to have important functions under freshwater conditions (Henry et al, 2012).…”

“…Understanding the molecular basis and ontogeny of this process, therefore, is of great interest to evolutionary biologists. At present, one of the most species rich crustacean groups is the genus Macrobrachium that includes 258 described species worldwide and have been broadly categorized into two ecological groups: ALD (abbreviated larval development) and ELD (extended larval development) types, where ELD species require brackish or sea water to complete larval development and this process potentially involves many larval developmental stages (6-14) for up to 2-12 weeks or longer (Jalihal et al, 1993;Wowor et al, 2009;McNamara et al, 2015). To date, only 25 ALD Macrobrachium species have been recognized globally, while all remaining species are recognized as ELD species (Vogt, 2013).…”

“…Phylogenetic studies of this genus have reported multiple clades suggesting at least nine independent invasions into freshwater from marine ancestors worldwide (Murphy and Austin, 2005;Wowor et al, 2009;Pileggi and Mantelatto, 2010). Currently, only 25 species are known to be able to complete entire life cycle in freshwater, and only a few species are known to inhabit brackish and/or sea water for whole life cycle (Wowor et al, 2009;McNamara et al, 2015). Depending on life history traits, Macrobrachium species are categorized into two groups: abbreviated larval development (ALD) type and extended larval development (ELD) type (Short, 2004).…”

“…It is evident that none of these ALD traits are present in ELD taxa or in their marine relatives (Vogt, 2013) indicating that these are very specific adaptive traits that have evolved with freshwater colonization. It is also widely accepted that ALD species are most likely to be the oldest invaders of freshwater because there has been sufficient time for their freshwater adaptation to be complete (McNamara et al, 2015). As such, freshwater adaptation in ELD species can be considered an ongoing process as they still require brackish/marine water to complete larval development (Pileggi and Mantelatto, 2010).…”