Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri.
ABSTRACT Temperature variations are known to modulate aging and life-history traits in poikilotherms as different as worms, flies and fish. In invertebrates, temperature affects lifespan by modulating the slope of age-dependent acceleration in death rate, which is thought to reflect the rate of age-related damage accumulation. Here, we studied the effects of temperature on aging kinetics, aging-related behavioural deficits, and age-associated histological markers of senescence in the short-lived fish Nothobranchius furzeri. This species shows a maximum captive lifespan of only 3 months, which is tied with acceleration in growth and expression of aging biomarkers. These biological peculiarities make it a very convenient animal model for testing the effects of experimental manipulations on life-history traits in vertebrates. Here, we show that (i) lowering temperature from 25 degrees C to 22 degrees C increases both median and maximum lifespan; (ii) life extension is due to reduction in the slope of the age-dependent acceleration in death rate; (iii) lowering temperature from 25 degrees C to 22 degrees C retards the onset of age-related locomotor and learning deficits; and (iv) lowering temperature from 25 degrees C to 22 degrees C reduces the accumulation of the age-related marker lipofuscin. We conclude that lowering water temperature is a simple experimental manipulation which retards the rate of age-related damage accumulation in this short-lived species.
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ABSTRACT: African annual fishes from the genus Nothobranchius are small teleosts that inhabit temporary water bodies subject to annual desiccation due to the alternation of the monsoon seasons. Given their unique biology, these fish have emerged as a model taxon in several biological disciplines. Their increasing popularity stems from the extremely short lifespan that is the result of their specific life-history adaptations and is retained under laboratory conditions. Nothobranchius furzeri, the most popular laboratory species, is the vertebrate species with the shortest lifespan recorded in captivity. In the laboratory, adults of different Nothobranchius species and populations live between 3 and 18 months and, notably, there is a negative correlation between the captive lifespan of a species and the aridity of their habitat. Their short lifespan is coupled to rapid age-dependent functional decline and expression of cellular and molecular changes comparable to those observed in other vertebrates, including humans. The recent development of transgenesis in this species makes it possible to insert specific constructs into their genome, and the establishment of transgenic lines is facilitated by their very rapid generation time, which can be as short as 1 month. This makes Nothobranchius species particularly suited for investigating biological and molecular aspects of ageing and ageing-associated dysfunctions. At the same time, they also represent a unique model taxon to investigate the evolution of life-history adaptations and their genetic architecture. We review their natural history, including phylogenetic relationships, distribution in relation to habitat conditions and natural selection for differential longevity, population structure and demography, and life cycle with emphasis on diapause that may occur at three stages during embryonic development. We further critically evaluate their use as a laboratory model for understanding the evolution of a rapid ageing rate and its consequences for other life-history traits, for cellular, molecular and integrative traits associated with the ageing process, high incidence of neoplasias, their utility for genome-wide gene-expression studies, and as a model for quantitative genetics. We summarize recent achievements in fostering Nothobranchius species as a widely applicable model system, including an annotated transcriptome, successful transgenesis, and existence of viable inbred lines. We compare the conditions they experience in the wild and in captivity and suggest that they are an ideal taxon to investigate natural genetic variation in a laboratory setting. We conclude that Nothobranchius species - and N. furzeri in particular - could become a unique model taxon that bridges interests in ecological and biomedical research. We hope that a conceptual and methodological integration of these two branches of biology will provide important new insights. © 2015 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.Biological Reviews 04/2015; DOI:10.1111/brv.12183 · 9.79 Impact Factor
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ABSTRACT: Ambient temperature reduction (ATR) can extend the lifespan of organisms, but the underlying mechanism is poorly understood. In this study, cellular degradation activity was evaluated in the muscle of an annual fish (Nothobranchius rachovii) reared under high (30 °C), moderate (25 °C), and low (20 °C) ambient temperatures. The results showed the following: (i) the activity of the 20S proteasome and the expression of polyubiquitin aggregates increased with ATR, whereas 20S proteasome expression did not change; (ii) the expression of microtubule-associated protein 1 light chain 3-II (LC3-II) increased with ATR; (iii) the expression of lysosome-associated membrane protein type 2a (Lamp 2a) increased with ATR, whereas the expression of the 70-kD heat shock cognate protein (Hsc 70) decreased with ATR; (iv) lysosome activity increased with ATR, whereas the expression of lysosome-associated membrane protein type 1 (Lamp 1) did not change with ATR; and (v) the expression of molecular target of rapamycin (mTOR) and phosphorylated mTOR (p-mTOR) as well as the p-mTOR/mTOR ratio did not change with ATR. These findings indicate that ATR activates cellular degradation activity, constituting part of the mechanism underlying the longevity-promoting effects of ATR in N. rachovii.Age 04/2015; 37(2):9775. DOI:10.1007/s11357-015-9775-z · 3.45 Impact Factor
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ABSTRACT: An annual life cycle is characterized by growth, maturity, and reproduction condensed into a single, short season favourable to development, with production of embryos (seeds, cysts, or eggs) capable of surviving harsh conditions which juveniles or adults cannot tolerate. More typically associated with plants in desert environments, or temperate-zone insects exposed to freezing winters, the evolution of an annual life cycle in vertebrates is fairly novel. Killifish, small sexually dimorphic fishes in the Order Cyprinodontiformes, have adapted to seasonally ephemeral water bodies across much of Africa and South America through the independent evolution of an annual life history. These annual killifish produce hardy desiccation-resistant eggs that undergo diapause (developmental arrest) and remain buried in the soil for long periods when fish have perished due to the drying of their habitat. Killifish are found in aquatic habitats that span a continuum from permanent and stable to seasonal and variable, thus providing a useful system in which to piece together the evolutionary history of this life cycle using natural comparative variation. I first review adaptations for life in ephemeral aquatic environments in killifish, with particular emphasis on the evolution of embryonic diapause. I then bring together available evidence from a variety of approaches and provide a scenario for how this annual life cycle evolved. There are a number of features within Aplocheiloidei killifish including their inhabitation of marginal or edge aquatic habitat, their small size and rapid attainment of maturity, and egg properties that make them particularly well suited to the colonization of ephemeral waters. © 2015 Cambridge Philosophical Society.Biological Reviews 05/2015; DOI:10.1111/brv.12194 · 9.79 Impact Factor