Fluctuating temperatures extend median lifespan, improve reproduction and reduce growth in turquoise killifish

Highlights

• The effect of natural temperature fluctuations on vertebrate lifespan is unknown.

• Fluctuating temperatures extended lifespan in Nothobranchius furzeri killifish.

• Fluctuating temperatures reduced body size but increased relative fish fecundity.

• Life histories in stable temperatures are poor representation of natural conditions.

Abstract

In natural populations, individuals experience daily fluctuations in environmental conditions that synchronise endogenous biorhythms. Artificial alterations of environmental fluctuations can have negative consequences for life history traits, including lifespan. In laboratory studies of aging, the role of fluctuating temperature is usually overlooked and we know little of how thermal fluctuation modulates senescence in vertebrates. In this longitudinal study we followed individually-housed turquoise killifish, Nothobranchius furzeri, from two thermal regimes; ecologically relevant diel fluctuations (20 °C - 35 °C) and stable temperature (27.5 °C), and compared their survival, growth and reproduction. Fish experiencing fluctuating temperatures had a longer median lifespan but reached smaller asymptotic body size. Within-treatment variation indicated that extended lifespan in fluctuating temperatures was not causally linked to decreased growth rate or smaller body size, but occurred solely due to the effect of thermal fluctuations. Male body size was positively associated with lifespan in stable temperatures but this relationship was disrupted in fluctuating thermal regimes. Females exposed to fluctuating temperatures effectively compensated egg production for their smaller size. Thus, there was no difference in absolute fecundity between thermal regimes and body-size corrected fecundity was higher in females in fluctuating temperatures. Overall, despite a brief exposure to sub-optimal thermal conditions during fluctuations, fluctuating temperature had a positive effect on survival and reproduction. These results suggest that the expression of life history traits and their associations under stable temperatures are a poor representation of the relationships obtained from ecologically relevant thermal fluctuations.

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.