Fluctuating temperatures extend median lifespan, improve reproduction and reduce growth in turquoise killifish
Introduction
Environmental conditions modulate most organismal functions, from gene expression to behaviour (Fraser et al., 1993; Podrabsky and Somero, 2004). Temperature, light intensity and food availability fluctuate in predictable daily and seasonal cycles and organisms adapt their endogenous biorhythms to optimize performance (Claireaux and Lefrançois, 2007; Dillon et al., 2016). On the other hand, environmental fluctuation exposes organisms to periods of suboptimal conditions which may have negative consequences for survival (Zhang et al., 2018). Artificial desynchronization of environmental fluctuation may cause stress with long-term, senescence-related consequences (Almaida-Pagán et al., 2018). While high levels of stress may induce immediate mortality, mild stress typically has life-extending effects (Gems and Partridge, 2008). Organisms that have evolved under chronic environmental fluctuation are expected to possess efficient stress-coping adaptations (Angilletta, 2009; Kern et al., 2015).
Temperature has a fundamental effect on lifespan and low body temperature is associated with longer lifespan in both ectotherms and endotherms (Flouris and Piantoni, 2015; Keil et al., 2015). In ectothermic vertebrates, chronic exposure to sub-optimal temperatures (i.e. temperatures outside the range of preferred body temperatures (Gvoždík, 2018)) has been studied particularly in fishes (Keil et al., 2015), confirming their role in lifespan extension. However, the effect on other life history traits was negative as a consequence of lower metabolism and slower development rate (Angilletta, 2009). The role of fluctuating temperatures on lifespan is less clear (Colinet et al., 2015). Fluctuating temperatures and their effect on lifespan have been studied primarily in invertebrates such as nematodes, crustaceans (Daphnia sp) or insects and variously demonstrated lifespan extension, reduction or no effect (Cedergreen et al., 2016; Colinet et al., 2015; Schwartz et al., 2016). The lifespan modulating effect of fluctuating temperature remains largely untested in vertebrates, while both negative and positive effects of fluctuating temperature have been demonstrated on developmental rate (Kern et al., 2015; Niehaus et al., 2012), growth rate (Diana, 1984; Vondracek et al., 1988) and reproduction (Boulé and Fitzgerald, 1989; Podrabsky et al., 2008).
Growth and reproduction are commonly linked to survival via trade-off in resource allocation (Kirkwood, 1977; Lee et al., 2013), antagonistic pleiotropic genetic effects (Williams, 1957) or positive pleiotropic effects (Maklakov et al., 2015). From an evolutionary perspective, it is important to study growth and reproduction together with survival to obtain more complete information on the functional senescence of an organism (Lemaître and Gaillard, 2017; Monaghan et al., 2008). At least in insects, there appears to be no consistent link between survival and other life history traits across studies that exposed animals to fluctuating temperatures (reviewed in Colinet et al. (2015)). This is likely due to wide variation in the distance between the range of preferred body temperatures and the fluctuations tested, unpredictability of extrapolation from studies in stable temperature, and species-specific thermal sensitivity of traits examined (Colinet et al., 2015; Kingsolver et al., 2008; Niehaus et al., 2012). To our knowledge, the extent to which fluctuating temperatures contribute to modification of lifespan and its association with fundamental life history traits in vertebrates is unknown.
In the present study, we used the short-lived turquoise killifish Nothobranchius furzeri, a promising vertebrate model for aging (Hu and Brunet, 2018), to examine the role of fluctuating temperature on vertebrate lifespan and its relationship to thermally sensitive life history traits – growth and reproduction.
Section snippets
Study species
The turquoise killifish Nothobranchius furzeri is adapted to thermally challenging ephemeral savanna pools in south-east Africa and has a naturally short lifespan of several months (Reichard and Polačik, 2019). During the peak season of killifish abundance, water temperature in ephemeral savanna pools fluctuates in an asymptote of 15–20 °C daily, usually from 22 °C in the early morning to 38 °C in late afternoon (Žák et al., 2018). Perhaps as an adaptation to a thermally unstable environment,
Effect of thermal regime on lifespan
Fish in fluctuating temperatures had a 93% longer median lifespan than fish kept in stable temperature (log-rank, χ12 = 6.3, p = 0.010, N = 84, Fig. 2a). A longer median lifespan in fluctuating temperatures was recorded in males (χ12 = 5.4, p = 0.020, N = 44) but this difference, although numerically larger, was non-significant in females (χ12 = 1.5, p = 0.200, N = 40, Fig. 2b). Overall, median lifespan did not differ significantly between males and females within thermal regimes (fluctuating: χ
Discussion
Previous studies have detected a detrimental effect of stable temperature on early development of ectothermic vertebrates (Ashmore and Janzen, 2003; Niehaus et al., 2012). Using the short-lived fish Nothobranchius furzeri, we demonstrated that stable temperature shortened lifespan and decreased relative fecundity, but increased growth rate compared to individuals experiencing fluctuating temperatures.
Chronic exposure to stable temperature shortened the median lifespan of turquoise killifish
CRediT authorship contribution statement
Conceptualization: JZ, MR.
Data curation: JZ, MR.
Formal analysis: JZ.
Funding acquisition: MR, JZ.
Investigation: JZ.
Methodology: JZ, MR.
Project administration: MR, JZ.
Resources: MR.
Supervision: MR.
Validation: JZ, MR.
Visualization: JZ.
Writing - original draft: JZ, MR.
Writing - review & editing: JZ, MR.
Acknowledgements
We thank Vašek Homolka, Jiří Farkač and all other members of Reichard-Lab who helped with maintenance of the killifish colony. We thank Rowena Spence for English correction and Lumír Gvoždík, Radim Blažek, Lisandrina Mari, Matej Polačik and Milan Vrtílek for helpful comments on early version of the manuscript. All experimental procedures were in accordance with institutional and national laws.
Funding
This study was supported by Czech Science Foundation grant (19-01781S). The work of Jakub Žák from Department of Zoology, Faculty of Science at Charles University, Prague, was partially supported by SVV 260571/2020.
Data availability
Data and R code for the analyses are available at Figshare (doi: https://doi.org/10.6084/m9.figshare.12546632).
Declaration of competing interest
The authors declare no conflict of interests.
References (65)
- et al.
Flies evolved small bodies and cells at high or fluctuating temperatures
Ecol. Evol.
(2016) - et al.
Impact of a shift work-like lighting schedule on the functioning of the circadian system in the short-lived fish Nothobranchius furzeri
Exp. Gerontol.
(2018) Thermal Adaptation. A Theoretical and Empirical Synthesis
(2009)- et al.
Phenotypic variation in smooth softshell turtles (Apalone mutica) from eggs incubated in constant versus fluctuating temperatures
Oecologia
(2003) - et al.
Fish body sizes change with temperature but not all species shrink with warming
Nat. Ecol. Evol.
(2020) - et al.
Mitochondrial reactive oxygen species production by fish muscle mitochondria: potential role in acute heat-induced oxidative stress
Comp. Biochem. Physiol. Part B
(2016) - et al.
Fitting linear mixed-effects models using {lme4}
J. Stat. Softw.
(2015) - et al.
Longitudinal RNA-seq analysis of vertebrate aging identifies mitochondrial complex I as a small-molecule-sensitive modifier of lifespan
Cell Syst
(2016) - et al.
Consequences of circadian fluctuations in water temperature on the standard metabolic rate of Atlantic salmon parr (Salmo salar)
Can. J. Fish. Aquat. Sci.
(2013) - et al.
Rapid growth, early maturation and short generation time in African annual fishes
Evodevo
(2013)
Effects of constant and fluctuating temperatures on egg production in the threespine stickleback (Gasterosteus aculeatus)
Can. J. Zool.
Variable temperature stress in the nematode Caenorhabditis elegans (Maupas) and its implications for sensitivity to an additional chemical stressor
PLoS One
From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology
Biol. Rev.
Linking environmental variability and fish performance: integration through the concept of scope for activity
Philos. Trans. R. Soc. B Biol. Sci
Insects in fluctuating thermal environments
Annu. Rev. Entomol.
The growth of largemouth bass, Micropterus salmoides (Lacepede), under constant and fluctuating temperatures
J. Fish Biol.
Life in the frequency domain: the biological impacts of changes in climate variability at multiple time scales
Integr. Comp. Biol.
Links between thermoregulation and aging in endotherms and ectotherms
Temperature
Warming-induced reductions in body size are greater in aquatic than terrestrial species
Proc. Natl. Acad. Sci.
An R Companion to Applied Regression
Temperature-dependent switch between diurnal and nocturnal foraging in Salmon
Proc. R. Soc. B Biol. Sci.
Stress-response hormesis and aging: "that which does not kill us makes us stronger."
Cell Metab.
Annual fishes of the genus Nothobarnchius as a model system for aging research
Aging Cell
Life stage dependent responses to desiccation risk in the annual killifish Nothobranchius wattersi
J. Fish Biol.
Just what is the thermal niche?
Oikos
Economic thermoregulatory response explains mismatch between thermal physiology and behaviour in newts
J. Exp. Biol.
The African turquoise killifish: a research organism to study vertebrate aging and diapause
Aging Cell
A shift to organismal stress resistance in programmed cell death mutants
PLoS Genet.
Being cool: how body temperature influences ageing and longevity
Biogerontology
Physiological responses of ectotherms to daily temperature variation
J. Exp. Biol.
Environmental variation and selection on performance curves
Integr. Comp. Biol.
Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta
Evolution
Cited by (13)
Negative effects of fluctuating temperatures around the optimal temperature on reproduction and survival of the red flour beetle
2022, Journal of Thermal BiologyCitation Excerpt :Like previous studies on insects, our results generally indicate that fluctuations around the optimal temperatures are negative (Bozinovic et al., 2011; Małek et al., 2015). Regarding reproduction, the effect of fluctuating temperatures is not universal, and fluctuations may either increase or decrease reproduction (e.g., cf. Schwartz et al., 2016; Žák and Reichard, 2020). Colinet et al. (2015) suggest that it depends on whether the fluctuations include stressful temperatures.
Challenges in keeping annual killifish
2021, Laboratory Fish in Biomedical Research: Biology, Husbandry and Research Applications for Zebrafish, Medaka, Killifish, Cavefish, Stickleback, Goldfish and Danionella TranslucidaFluctuating and Stable High Temperatures Differentially Affect Reproductive Endocrinology of Female Pupfish
2024, Integrative Organismal BiologyDetection of genetic variation in bovine CRY1 gene and its associations with carcass traits
2023, Animal BiotechnologyOf telomeres and temperature: Measuring thermal effects on telomeres in ectothermic animals
2022, Molecular Ecology