Ontogeny of osmoregulation in postembryonic fish: A review

Varsamos, Stamatis; Nebel, Catherine; Charmantier, Guy

doi:10.1016/j.cbpb.2005.01.013

Cited by 342 publications

(266 citation statements)

References 216 publications

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“…For example, fishes osmoregulate via their gills and kidneys, which contain an abundant supply of CRMs (26,27), similar to those that regulate ion concentration in the brood pouch during gestation. Therefore, it is possible that meprins, cimp1, nephrosin, and patristacin, a group of closely related metalloproteases expressed in organs with CRMs, all perform a function in osmoregulation.…”

Section: Resultsmentioning

confidence: 99%

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

Proc. Natl. Acad. Sci. U.S.A.

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Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the proteins they encode, or both. Here we present an astacin metalloprotease, dubbed patristacin, which has been coopted without duplication, via alteration in the expression of a preexisting gene from the kidney and liver of bony fishes, for a novel role in the brood pouch of pregnant male pipefish. We examined the molecular evolution of patristacin and found conservation of astacin-specific motifs but also several positively selected amino acids that may represent functional modifications for male pregnancy. Overall, our results pinpoint a clear case in which gene cooption occurred without gene duplication during the genesis of an evolutionarily significant novel structure, the male brood pouch. These findings contribute to a growing understanding of morphological innovation, a critically important but poorly understood process in evolutionary biology.novel trait evolution ͉ patristacin ͉ Syngnathidae E volutionary innovation has been defined as ''the origin of a novel body part which may serve a novel function or specialize in a function that was already performed in the ancestral lineage but without a dedicated organ' ' (ref. 1, p. 581). In seahorses and pipefishes (family Syngnathidae) males carry their embryos on their ventral surface, either exposed to the environment or enclosed in a fleshy brood pouch (Fig. 1). The brood pouch is a clear example of an evolutionary innovation: syngnathids are the only lineage to have evolved a morphological structure that allows males to become pregnant. In many species of syngnathid fishes, the brood pouch is a complex organ composed of highly vascularized epithelial tissue that forms a honeycomb matrix encapsulating individual eggs during gestation ( Fig. 1) (2). This placenta-like tissue apparently supplies nutrients to developing embryos (3) in a manner analogous to the placenta of female mammals. The pouch is lined with cells rich in mitochondria (CRMs) (Fig. 1) (2, 4) that transfer ions between the brood pouch fluid and the male bloodstream, maintaining an osmotically neutral environment during the early stages of gestation (4-6). A phylogeny of the Syngnathidae suggests two independent origins of the brood pouch based on its location on either the abdomen (Gastrophori) or the tail (Urophori) of the male (7), and within these two lineages there is considerable variation in the degree to which the pouch encloses developing embryos, the complexity of the ''pseudoplacenta,'' and the structure of brood pouch folds (7).Clearly, the evolution of a structure as complex as a brood pouch req...

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Section: Resultsmentioning

confidence: 99%

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Harlin-Cognato

Hoffman

Jones

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, most marine fish larvae (such as the flatfishes discussed above) are planktonic and transform into juveniles that either swim in the water column or are benthic (Leis, 2006). In freshwater populations, metamorphosis is also morphologically obvious, as seen in the alteration of the zebrafish fins and gut (Brown, 1997), or salmonid smoltification (Varsamos et al, 2005).…”

Section: Diversity Of Chordate Metamorphosesmentioning

confidence: 99%

The history of a developmental stage: Metamorphosis in chordates

Paris

Laudet

2008

Genesis

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Summary: Metamorphosis displays a striking diversity in chordates, a deuterostome phylum that comprises vertebrates, urochordates (tunicates), and cephalochordates (amphioxus). In anuran amphibians, the tadpole loses its tail, develops limbs, and undergoes profound changes at the behavioral, physiological, biochemical, and ecological levels. In ascidian tunicates, the tail is lost and the head tissues are drastically remodeled into the adult animal, whereas in amphioxus, the highly asymmetric larva transforms into a relatively symmetric adult. This wide diversity has led to the proposal that metamorphosis evolved several times independently in the different chordate lineages during evolution. However, the molecular mechanisms involved in metamorphosis are largely unknown outside amphibians and teleost fishes, in which metamorphosis is regulated by the thyroid hormones (TH) T 3 and T 4 binding to their receptors (thyroid hormone receptors). In this review, we compare metamorphosis in chordates and then propose a unifying definition of the larva-to-adult transition, based on the conservation of the role of THs and some of their derivatives as the main regulators of metamorphosis. According to this definition, all chordates (if not, all deuterostomes) have a homologous metamorphosis stage during their postembryonic development. The intensity and the nature of the morphological remodeling varies extensively among taxa, from drastic remodeling like in some ascidians or amphibians to more subtle events, as in mammals. genesis 46:657-672,

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“…Osmoregulatory capacity in marine fish larvae generally increases during ontogeny, and it is therefore likely that the low tolerance of early larval barramundi to potassium deficiency is linked to their reduced osmoregulatory capacity (Varsamos et al, 2005). suggested that juvenile barramundi may regulate their drinking rate in potassium-deficient water in an effort to increase uptake.…”

Section: Resultsmentioning

confidence: 99%

“…suggested that juvenile barramundi may regulate their drinking rate in potassium-deficient water in an effort to increase uptake. Although it has been shown that pre-feeding marine fish larvae actively drink seawater, (Mangor-Jensen and Adoff, 1987;Tytler and Blaxter, 1988;Varsamos et al, 2004), it is generally accepted that they lack the ability of juveniles and adults to regulate their drinking rate in response to changing salinity (Varsamos et al, 2005). With weight-normalised drinking rates typically increasing during development (MangorJensen and Adoff, 1987;Miyazaki et al, 1998;Reitan et al, 1998), this may represent a mechanism for increased uptake of potassium as larvae develop.…”

Section: Resultsmentioning

confidence: 99%

Larval rearing of barramundi (Lates calcarifer) in saline groundwater

2008

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Barramundi (Lates calcarifer) larvae were reared from 2 to 25 days post hatch in 14‰ saline groundwater with either no potassium supplementation (38% K-equivalence) or full potassium supplementation (100% K-equivalence). Growth, survival and swimbladder inflation of these larvae were compared against those grown in control treatments of seawater (32‰) and seawater diluted to 14‰. Those reared in saline groundwater with 38% K-equivalence exhibited complete mortality within 2 days, while those held in groundwater with full supplementation survived at a rate equal to both control treatments (pooled average 51.1 ± 0.5%). At 25 days post hatch, there was no significant difference in larval length or dry weight between those grown in the 14‰ control treatment and those in the saline groundwater with full potassium supplementation. There were no significant differences in swim bladder inflation between any of the surviving treatments (average 93.3 ± 2.5%). This is the first description of rearing barramundi larvae both in low salinity seawater and in saline groundwater and demonstrates that the requirement for potassium by larval barramundi is higher than for juveniles of the same species.

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Ontogeny of osmoregulation in postembryonic fish: A review

Cited by 342 publications

References 216 publications

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

The history of a developmental stage: Metamorphosis in chordates

Larval rearing of barramundi (Lates calcarifer) in saline groundwater

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