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Survivorship curves for 11 strains of Brachionus grown under high (red, 21 °C) and low (blue, 16 °C) temperature, and for B. manjavacas RUS (BmanRUS) grown under ad libitum (solid line), or chronic caloric restriction (dashed line) food conditions. For each strain, survivorship at 16 °C was significantly different than at 21 °C (Mantel-Cox test, p < 0.0003) except for AUBUS001 (p = 0.012), JPNAG062 (p = 0.026) and BpL1 (p = 0.149).
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Lifespan extension under low temperature is well conserved across both endothermic and exothermic taxa, but the mechanism underlying this change in aging is poorly understood. Low temperature is thought to decrease metabolic rate, thus slowing the accumulation of cellular damage from reactive oxygen species, although recent evidence suggests involv...
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... Brachionus rotifers at 21 °C and 16 °C. We observed a high degree of variability in the response to low temperature among these congeneric strains. When grown at 21 °C under ad libitum food conditions, median lifespan varied from 10 d to 33.5 d among the 11 strains; minimum lifespan was 2 days, while maximum lifespan ranged from 14.7 to 33.6 d ( Fig. 1; Table S1). With continuous growth at 16 °C, median lifespan increased by 6%-100% in nine strains (p = 0.0001), decreased by 6% in one strain (JPNAG062; p = 0.0001), and did not change in one strain (BpL1; p = 0.15). While both median and maximum lifespan at 21 °C were positively correlated with lifespan at 16 °C, there was no corre- ...
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... p = 0.15). While both median and maximum lifespan at 21 °C were positively correlated with lifespan at 16 °C, there was no corre- lation between lifespan at 21 °C and the percent change in lifespan with growth at 16 °C (Fig. 2). There was no correlation between latitude of origin and lifespan at 21 °C, 16 °C, or percent change in lifespan ( Fig. S1; linear regression; R 2 < 0.04 for all comparisons). Comparison of the rate of aging at 16 °C and 21 °C, measured as the slope of the Gompertz regression, showed significant differences in the rate of aging for all 11 strains (Sum-of-squares F test, p < 0.05; Fig. 3, Table S1). Changes in the slope of the Gompertz regression better re- ...
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... determine if lifespan effects of caloric restriction and low tem- perature were additive, we tested BmanRUS under a combination of low temperature and CCR. Median lifespan increased by 60% under low temperature alone, 13% under CCR alone, and by 80% under the combination of low temperature and CR (Table S1; Fig. 1). Maximum lifespan was significantly increased by low temperature, but not by ...
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In this article, we review the main theories of biological aging, exploring the interaction of genetic, epigenetic, metabolic, immunological, and ecological factors in this process. For this purpose, we examine and discuss theories such as the allocation of metabolic resources, pleiotropic antagonism, genetic regulation, codon restriction, replicat...
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... The body expends more energy for excess protein digestion because protein increases thermogenetic effect up to 25% of total energy expenditure [26]. Increased MR leads to decreased lifespan [29,75]. ...
... Daphnia reared under colder conditions exhibit a longer lifespan compared to those in warmer conditions (Adamczuk, 2020;MacArthur & Baillie, 1929). Further studies are needed to investigate molecular mechanisms of temperature-dependent lifespan change (Gribble et al., 2018). We also found that the gene EIF4EBP2 (one of four candidate genes involved in the GO term "translation repressor activity") encodes a protein that is a crucial component of the target of the rapamycin (TOR) signalling pathway, which could regulate multiple transcriptional pathways in response to heat stress (Aramburu et al., 2014). ...
Climate is a fundamental abiotic factor that plays a key role in driving the evolution, distribution and population diversification of species. However, there have been few investigations of genomic signatures of adaptation to local climatic conditions in cladocerans. Here, we have provided the first high-quality chromosome-level genome assembly (~143 Mb, scaffold N50 12.6 Mb) of the waterflea, Daphnia galeata, and investigated genomic variation in 22 populations from Central Europe and Eastern China. Our ecological-niche models suggested that the historic distribution of D. galeata in Eurasia was significantly affected by Quaternary climate fluctuations. We detected pronounced genomic and morphometric divergences between European and Chinese D. galeata populations. Such divergences could be partly explained by genomic signatures of thermal adaptation to distinct climate regimes: a set of candidate single-nucleotide polymorphisms (SNPs) potentially associated with climate were detected. These SNPs were in genes significantly enriched in the Gene ontology terms "determination of adult lifespan" and "translation repressor activity", and especially, mthl5 and SOD1 involved in the IIS pathway, and EIF4EBP2 involved in the target of the rapamycin signalling pathway. Our study indicates that certain alleles might be associated with particular temperature regimes, playing a functional role in shaping the population structure of D. galeata at a large geographical scale. These results highlight the potential role of molecular variation in the response to climate variation, in the context of global climate change.
... For instance, if hot temperatures increased expected future mortality rates, this could lead to females terminally investing in early adult life reproduction (Clutton-Brock, 1984). This increased early adult life investment would in turn lead to fewer eggs being available for laying later, which results in a less equal distribution of eggs over a female's life span, leading to faster senescence (e.g., Gribble et al, 2018). ...
Developmental and adult environments can interact in complex ways to influence the fitness of individuals. Most studies investigating effects of the environment on fitness focus on environments experienced and traits expressed at a single point in an organism's life. However, environments vary with time, so the effects of the environments that organisms experience at different ages may interact to affect how traits change throughout life. Here we test whether thermal stress experienced during development leads individuals to cope better with thermal stress as adults. We manipulated temperature during both development and adulthood and measured a range of life‐history traits, including senescence, in male and female seed beetles (Callosobruchus maculatus). We found that thermal stress during development reduced adult reproductive performance of females. In contrast, lifespan and age‐dependent mortality were affected more by adult than developmental environments, with high adult temperatures decreasing longevity and increasing age‐dependent mortality. Aside from an interaction between developmental and adult environments to affect age‐dependent changes in male weight, we did not find any evidence of a beneficial acclimation response to developmental thermal stress. Overall, our results show that effects of developmental and adult environments can be both sex‐ and trait‐ specific, and that a full understanding of how environments interact to affect fitness and ageing requires the integrated study of conditions experienced during different stages of ontogeny. This article is protected by copyright. All rights reserved
... Some of the physiological stresses experienced by individuals during hibernation are similar to those observed with aging, and therefore the molecular and physiological responses required for an individual to successfully hibernate may prevent aging 36,46 . Additionally, hibernation combines conditions known to promote longevity 36,46,93 , such as food deprivation (calorie restriction [94][95][96] ), low body temperature 93,[97][98][99] , and reduced metabolic rates 46 . Conceivably, these factors may also be associated with the slower marmot aging observed in the beginning and end of their active season drop food consumption by 55% prior to hibernation 105 , and some species exhibit short and shallow torpor bouts before and after hibernation 106 . ...
Species that hibernate live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor-arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause aging suppression. Metabolic rate is also a known correlate of longevity, we thus proposed the ‘hibernation-aging hypothesis’ whereby aging is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7-8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females was modeled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic age change over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (2-years old). With respect to circannual patterns, the epigenetic age increased during the summer and essentially stalled during the winter. Our enrichment analysis of age-related CpG sites revealed pathways related to development and cell differentiation, while the season-related CpGs enriched pathways related to central carbon metabolism, immune system, and circadian clock. Taken together, our results are consistent with the hibernation-aging hypothesis and may explain the enhanced longevity in hibernators.
... Some of the physiological stresses experienced by individuals during hibernation are similar to those observed with aging, and therefore the molecular and physiological responses required for an individual to successfully hibernate may prevent aging 36,45 . Additionally, hibernation combines conditions known to promote longevity 36,45,82 , such as food deprivation (calorie restriction [83][84][85], low body temperature 82,[86][87][88] , and reduced metabolic rates 45 . Conceivably, these factors may also be associated with the slower marmot aging observed in the beginning and end of their active season ( Figure 2B). ...
Species that hibernate live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor-arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause aging suppression. Metabolic rate is also a known correlate of longevity, we thus proposed the hibernation-aging hypothesis whereby aging is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7-8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females were modeled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic age change over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (2-years old). With respect to circannual patterns, the epigenetic age increased during the summer and essentially stalled during the winter. Our enrichment analysis of age-related CpG sites revealed pathways related to development and cell differentiation, while the season-related CpGs enriched pathways related to central carbon metabolism, immune system, and circadian clock. Taken together, our results are consistent with the hibernation-aging hypothesis and may explain the enhanced longevity in hibernators.
... Animals maintained at lower temperatures also displayed reduced reproduction but an extended reproductive period (Brys, Vanfleteren, & Braeckman, 2007). The effect of temperature on rotifer lifespan appears to vary by strain; when 11 strains were examined some showed as much as a doubling in lifespan while others showed as little as a 6% increase (Gribble et al., 2018). • Antioxidants. ...
Invertebrate model organisms represent an invaluable tool for the biology of aging research. They possess a number of advantages over vertebrate models in aging studies, including short lifespan, small size (a key advantage for large-scale lifespan investigations), ease of propagation, transparent bodies, and powerful genetics. These organisms also present advantages as simplified animal models enabling the study of individual processes. Studies using invertebrate models to investigate the biology of aging have primarily used the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster. In this chapter, we the relative benefits and challenges in using these models as well as the tools these organisms contribute to aging research. Finally, a number of other invertebrate models have been developed, each with its own key advantages. These other invertebrate models are described in the third part of this chapter along with research done in these systems in the biology of aging.
... Each Brachionus species comprises a diversity of strains; these strains evolved in varied environments where they were subject to different diet, temperature, salinity, predation, hydroperiodicity, and pathogen selective pressures, leading to natural genetic and phenotypic variability. These different strains have diverse aging phenotypes and responses to aging interventions and thus function as "natural mutants" that can be used in comparative investigations to identify mechanisms driving aging and interventions [28,79,80]. Decades of work by dozens of research groups have characterized shifts in lifespan, health, and reproduction in response to altered environmental conditions and have revealed significant variability in aging plasticity among Brachionus strains. ...
... Responses to a range of other treatments, including low temperature [80,83,84] and pharmaceuticals [58], range from positive to negative among Brachionus genotypes. In a survey of 11 closely-related strains, growth at low temperature led to changes in lifespan ranging from a 6% decrease to a 100% increase, depending on the strain [80]. ...
... Responses to a range of other treatments, including low temperature [80,83,84] and pharmaceuticals [58], range from positive to negative among Brachionus genotypes. In a survey of 11 closely-related strains, growth at low temperature led to changes in lifespan ranging from a 6% decrease to a 100% increase, depending on the strain [80]. These results suggest active genetic control of lifespan extension under low temperature, rather than a passive thermodynamic response that lowers metabolism and thereby slows the accumulation of ROS-related cellular damage, as has been hypothesized. ...
Because every species has unique attributes relevant to understanding specific aspects of aging, using a diversity of study systems and a comparative biology approach for aging research has the potential to lead to novel discoveries applicable to human health. Monogonont rotifers, a standard model for studies of aquatic ecology, evolutionary biology, and ecotoxicology, have also been used to study lifespan and healthspan for nearly a century. However, because much of this work has been published in the ecology and evolutionary biology literature, it may not be known to the biomedical research community. In this review, we provide an overview of Brachionus rotifers as a model to investigate nutritional and metabolic regulators of aging, with a focus on recent studies of dietary and metabolic pathway manipulation. Rotifers are microscopic, aquatic invertebrates with many advantages as a system for studying aging, including a two-week lifespan, easy laboratory culture, direct development without a larval stage, sexual and asexual reproduction, easy delivery of pharmaceuticals in liquid culture, and transparency allowing imaging of cellular morphology and processes. Rotifers have greater gene homology with humans than do established invertebrate models for aging, and thus rotifers may be used to investigate novel genetic mechanisms relevant to human lifespan and healthspan. The research on caloric restriction; dietary, pharmaceutical, and genetic interventions; and transcriptomics of aging using rotifers provide insights into the metabolic regulators of lifespan and health and suggest future directions for aging research. Capitalizing on the unique biology of Brachionus rotifers, referencing the vast existing literature about the influence of diet and drugs on rotifer lifespan and health, continuing the development of genetic tools for rotifers, and growing the rotifer research community will lead to new discoveries a better understanding of the biology of aging.
... Recently, studies have suggested that the mechanism of lifespan extension through low temperature is an active genetic process rather than a passive thermodynamic one and is dependent upon genotype. Additionally, a probable mechanism of lifespan extension by low temperature may work via non-or partially overlapping molecular pathways, e.g., by calorie restriction response [67]. Interestingly, in Drosophila short-term exposures to low temperatures lead to long-term increase in longevity and stress resistance, suggesting that it is not a short-term decrease in metabolism but rather a long-term physiological adaptation that controls lifespan [68]. ...
Despite many studies of the aging process, questions about key factors ensuring longevity have not yet found clear answers. Temperature seems to be one of the most important factors regulating lifespan. However, the genetic background may also play a key role in determining longevity. The aim of this study was to investigate the relationship between the temperature, genetic background (fruit fly origin), and metabolic rate on lifespan. Experiments were performed with the use of the wild type Drosophila melanogaster fruit flies originating from Australia, Canada, and Benin and the reference OregonR strain. The metabolic rate of D. melanogaster was measured at 20 °C, 25 °C, and 28 °C in an isothermal calorimeter. We found a strong negative relationship between the total heat flow and longevity. A high metabolic rate leads to increased aging in males and females in all strains. Furthermore, our results showed that temperature has a significant effect on fecundity and body weight. We also showed the usefulness of the isothermal calorimetry method to study the effect of environmental stress conditions on the metabolic activity of insects. This may be particularly important for the forecasting of impact of global warming on metabolic activity and lifespan of various insects.
Across diverse taxa, offspring from older mothers have decreased lifespan and fitness. Little is known about the extent to which maternal age effects vary among genotypes for a given species, however, except for studies of a few arthropod species. To investigate the presence and degree of intraspecific variability in maternal age effects, we compared lifespan, reproductive schedule, and lifetime reproductive output of offspring produced by young, middle‐aged, and old mothers in four strains of rotifers in the Brachionus plicatilis species complex. We found significant variability among strains in the magnitude and direction of maternal age effects on offspring life history traits. In one strain, offspring of young mothers lived 20% longer than offspring of old mothers, whereas there were no significant effects of maternal age on lifespan for other strains. Depending on strain, advanced maternal age had positive effects, negative effects, or no effect on lifetime reproductive output. Across strains, older mothers produced offspring that had higher maximum daily reproduction early in life. The effects of maternal age on offspring vital rates could not be explained by changes in trade‐offs between lifespan and reproduction. This study documents intraspecific variability in maternal age effects in an additional clade. Investigating intraspecific variability is critical for understanding the ubiquity of maternal age effects and their role in the evolution of life history and aging.
Flourishing recent comparative studies on senescence have revealed an uncovered diversity across the tree of life of the shapes of the age trajectories of mortality (actuarial senescence) and to a lesser extent of reproduction (reproductive senescence). Evolutionary theories have been called up to explain why some species suffer from positive senescence while others benefit from negligible or even negative senescence. We still know little about how, within a species, the shapes of the age trajectories of different traits are linked to each other and how they vary or covary depending on the genetic background and environmental conditions. We report here the results of an experimental study whose aim was to describe the actuarial and reproductive senescence in various genetically distinct lineages of a Collembola, a hexapod with indeterminate growth. We compared the age trajectories of individuals raised under two food regimes to study if and how the shapes of these age trajectories are plastically modified by environmental conditions. We found clear evidence of actuarial and reproductive senescence, especially when the springtails were fully fed. Clutch size increased as female become older and then declined progressively after reproduction reached a maximum. This age decline in fertility went along with a progressive slowing down of the pace of the egg-laying, a reduction of egg quality (more sterile eggs), while egg size undergoes little change with age. We found that the onset of reproductive decline occurred before the beginning of actuarial senescence, and show that escaping senescence is physiologically possible for certain lineages under dietary restricted conditions.
