Temperature affects longevity and age‐related locomotor and cognitive decay in the short‐lived fish Nothobranchius furzeri

Abstract

SummaryTemperature 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 agerelated 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 °°°° C to 22 °°°° 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 °°°° C to 22 °°°° C retards the onset of age-related locomotor and learning deficits; and (iv) lowering temperature from 25 °°°° C to 22 °°°° 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 agerelated damage accumulation in this short-lived species.

The African turquoise killifish: A research organism to study vertebrate aging and diapause

“…However, it is important to note that the turquoise killifish's fast‐aging process is unlikely to be just a pathological consequence of a progeria‐like state. First, this fish exhibit clear neurological aging phenotypes (declining neurogenesis and cognition; Tozzini et al., 2012; Valenzano, Terzibasi, Vattaneo et al., 2006a, 2006b), and those are not seen in progeria patient. Second, the cells from old killifish do not exhibit the irregular shape of nuclei that is characteristic of progeria (C.‐K.…”

“…Indeed, despite their short lifespan compared to other vertebrates, various strains of the turquoise killifish recapitulate numerous stereotypical aging traits that have been reported in other vertebrates (Figure 5), including decline in reproduction, fertility, cognition, mobility, regeneration, and tissue homeostasis, along with increased incidence of senescence, neural and muscular degeneration, and cancerous lesions (Di Cicco et al., 2011; Terzibasi, Valenzano & Cellerino, 2007; Terzibasi et al., 2008; Valenzano, Terzibasi, Cattaneo, Domenici & Cellerino, 2006; Wendler, Hartmann, Hoppe & Englert, 2015). Importantly, the turquoise killifish does not die of just one disease, but appears to have multiple causes of death in old age, indicating that its lifespan is truly compressed rather than limited by a specific disease.…”

“…The turquoise killifish provides a great opportunity to fill this gap, as its compressed lifespan requires fewer data points to capture the kinetics of the aging process (Baumgart et al., 2014). In addition, the turquoise killifish exhibits various complex behaviors such as learning that could be monitored and measured (Valenzano, Terzibasi, Vattaneo et al., 2006a, 2006b). Coupling the compressed aging process with systematic behavior analysis such as cognitive decline adds more information to aging studies.…”

“…The killifish short lifespan makes it feasible to precisely manipulate the environment over the same short experimental cycle. The lifespan of turquoise killifish is responsive to environmental stimuli that affect the rate of aging in virtually all species (e.g., dietary restriction [Terzibasi et al., 2009]), or in some species (e.g., temperature [Valenzano, Terzibasi, Vattaneo et al., 2006a, 2006b] and Resveratrol [Valenzano, Terzibasi, Genade et al., 2006]), making the turquoise killifish a great vertebrate research organism to systematically study the environmental inputs of aging. Its compressed lifecycle and short lifespan allow relatively high‐throughput lifespan experiments, thereby rendering the study of environmental influence, and its interplay with the genetic background, on aging more feasible.…”

Squeezing out the last egg—annual fish increase reproductive efforts in response to a predation threat

“…While the potential for phenotypic plasticity in the postembryonic life stages of Nothobranchius killifish has been demonstrated (Grégoir et al., 2017; Valenzano, Terzibasi, Cattaneo, Domenici, & Cellerino, 2006; Valenzano, Terzibasi, et al., 2006; Vrtílek & Reichard, 2015), the response of juvenile and adult individuals to predation risk by riverine fish is currently unknown. In other toothcarps, maturation could be plastically accelerated at the expense of somatic growth to increase the chances of reproductive success before being predated upon (Reznick, 1990).…”