Depth-selection behavior and longevity in Daphnia: an evolutionary test for the predation-avoidance hypothesis

The classic evolutionary theory of senescence predicts that long lifespan evolves under low risk of extrinsic mortality. As lakes present planktonic animals with vertical gradients of mortality risk associated with fish predation, we expected the individual lifespan of Daphnia of the “hypolymnetic” clones to be longer than that of “epilimnetic” Daphnia. In order to test this prediction, we performed a laboratory study on 14 clones from the D. longispina species complex, taken during the daytime either from epilimnion or hypolimnion of three mesotrophic lakes. “Epilimnetic” Daphnia started reproduction earlier, aged faster, and lived shorter than their “hypolimnetic” conspecifics. Our results indirectly support the predation-avoidance hypothesis as the ultimate explanation for depth-selection behavior in Daphnia.     

Metabolic rate affects adult life span independently of developmental rate in parasitoid wasps

Developmental time and body size correlate with lifespan in a wide range of taxa, although not in insect parasitoids. When the rate of development is independent of adult metabolic rate, adult lifespan is free to adapt to the adult environment. We suggest that interspecific variation in intrinsic adult metabolic rates, differences in allocation of lipids to longevity, and reproduction and differences in the ability to use carbohydrates as an adult should all result in variation of adult lifespan, independent of development time. To test these ideas, we measured metabolic rate, lipid content and egg load at eclosion, developmental time, and lifespan of females with and without carbohydrate food in five species of Asobara, which represent parasitoids of Drosophila. No relationship between development time and adult longevity was found. As predicted, metabolic rates varied between species and appeared to trade off with adult longevity. We found no clear link between initial egg load and the longevity of a species, suggesting that lipid allocation may be less important in determining adult lifespan. The results obtained indicate that differences in metabolic rate have an important effect on adult lifespan, without affecting developmental rate in parasitoids. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 45–56.     

Germline Signals Deploy NHR-49 to Modulate Fatty-Acid β-Oxidation and Desaturation in Somatic Tissues of C. elegans

In C. elegans, removal of the germline extends lifespan significantly. We demonstrate that the nuclear hormone receptor, NHR-49, enables the response to this physiological change by increasing the expression of genes involved in mitochondrial β-oxidation and fatty-acid desaturation. The coordinated augmentation of these processes is critical for germline-less animals to maintain their lipid stores and to sustain de novo fat synthesis during adulthood. Following germline ablation, NHR-49 is up-regulated in somatic cells by the conserved longevity determinants DAF-16/FOXO and TCER-1/TCERG1. Accordingly, NHR-49 overexpression in fertile animals extends their lifespan modestly. In fertile adults, nhr-49 expression is DAF-16/FOXO and TCER-1/TCERG1 independent although its depletion causes age-related lipid abnormalities. Our data provide molecular insights into how reproductive stimuli are integrated into global metabolic changes to alter the lifespan of the animal. They suggest that NHR-49 may facilitate the adaptation to loss of reproductive potential through synchronized enhancement of fatty-acid oxidation and desaturation, thus breaking down some fats ordained for reproduction and orchestrating a lipid profile conducive for somatic maintenance and longevity.     

Seasonal life history trade-offs in two leafwing butterflies: Delaying reproductive development increases life expectancy

Surviving inhospitable periods or seasons may greatly affect fitness. Evidence of this exists in the prevalence of dormant stages in the life cycles of most insects. Here I focused on butterflies with distinct seasonal morphological types (not a genetic polymorphism) in which one morphological type, or form, delays reproduction until favorable conditions return, while the other form develops in an environment that favors direct reproduction. For two butterflies, Anaea aidea and A. andria, I tested the hypothesis that the development of each seasonal form involves a differential allocation of resources to survival at eclosion. I assayed differences in adult longevity among summer and winter forms in either a warm, active environment or a cool, calm environment. Winter form adults lived 40 times longer than summer form but only in calm, cool conditions. The magnitude of this difference provided compelling evidence that the winter form body plan and metabolic strategy (i.e. resource conservatism) favor long term survival. This research suggests that winter form adults maintain lowered metabolic rate, a common feature of diapause, to conserve resources and delay senescence while overwintering.     

Investigations into depth and temperature habitat utilization and overwintering grounds of juvenile sandbar sharks, Carcharhinus plumbeus: the importance of near shore North Carolina waters

Defining the location and habitat characteristics of areas of aggregation of Atlantic shark species has been identified as an important information need for current and future management efforts. The primary objective of this project was to investigate the depths and temperatures of the waters occupied by large juvenile sandbar sharks of the northwest Atlantic population during the winter months and the overwintering localities of these animals using a fishery independent method. During the summer of 2003, 21 sandbar sharks captured in the Eastern Shore of Virginia bays and lagoons were outfitted with satellite transmitters that were programmed to detach during the following winter. The sharks occurred in significantly colder and deeper waters during the winter period than during the summer nursery period with a mean depth and temperature recorded by the transmitters during the winter period of 19.9°C and 20.8 m and a mean depth and temperature recorded during the summer period of 24.0°C and 4.3 m. Despite this decrease in temperature and increase in depth of occurrence, the sharks remained in relatively warm waters and shallow depths throughout the overwintering period. Satellite pop-off locations during the overwintering period were concentrated in central North Carolina coastal waters, where a unique combination of shallow depths and warm temperatures may contribute to the survivorship of these animals while they overwinter in these waters.     

ASM-3 Acid Sphingomyelinase Functions as a Positive Regulator of the DAF-2/AGE-1 Signaling Pathway and Serves as a Novel Anti-Aging Target

In C. elegans, the highly conserved DAF-2/insulin/insulin-like growth factor 1 receptor signaling (IIS) pathway regulates longevity, metabolism, reproduction and development. In mammals, acid sphingomyelinase (ASM) is an enzyme that hydrolyzes sphingomyelin to produce ceramide. ASM has been implicated in CD95 death receptor signaling under certain stress conditions. However, the involvement of ASM in growth factor receptor signaling under physiological conditions is not known. Here, we report that in vivo ASM functions as a positive regulator of the DAF-2/IIS pathway in C. elegans. We have shown that inactivation of asm-3 extends animal lifespan and promotes dauer arrest, an alternative developmental process. A significant cooperative effect on lifespan is observed between asm-3 deficiency and loss-of-function alleles of the age-1/PI 3-kinase, with the asm-3; age-1 double mutant animals having a mean lifespan 259% greater than that of the wild-type animals. The lifespan extension phenotypes caused by the loss of asm-3 are dependent on the functions of daf-16/FOXO and daf-18/PTEN. We have demonstrated that inactivation of asm-3 causes nuclear translocation of DAF-16::GFP protein, up-regulates endogenous DAF-16 protein levels and activates the downstream targeting genes of DAF-16. Together, our findings reveal a novel role of asm-3 in regulation of lifespan and diapause by modulating IIS pathway. Importantly, we have found that two drugs known to inhibit mammalian ASM activities, desipramine and clomipramine, markedly extend the lifespan of wild-type animals, in a manner similar to that achieved by genetic inactivation of the asm genes. Our studies illustrate a novel strategy of anti-aging by targeting ASM, which may potentially be extended to mammals.     

Longevity of <Emphasis Type="Italic">Daphnia magna</Emphasis> males and females

In many species, males are shorter-lived than females, and, mostly anecdotally, shorter lifespan was also attributed to Daphnia males. This does not necessarily stay in accordance with the biological roles of the sexes in Daphnia. Daphnia females maximize their fitness by maximizing the number of produced offspring, which incurs costs associated with quick attainment of large body size: metabolic costs of fast growth and increased risk of predation. In contrast, Daphnia males maximize fitness by maximizing the number of fertilized females, and seem to follow the strategy that enables them to maximize the lifetime female encounter rate, which should increase with lengthening lifespan. As arguments exist both in favour and against males living longer than females, we tested for differences in physiological lifespan of Daphnia magna males and females. Although maximum observed lifespan was always equal or longer in males than in females, no statistically significant differences were found. The results indicate that Daphnia males should not be considered short-lived anymore.     

The Good,the Bad and the Plenty: Interactive Effects of Food Quality and Quantity on the Growth of Different Daphnia Species

Effects of food quality and quantity on consumers are neither independent nor interchangeable. Although consumer growth and reproduction show strong variation in relation to both food quality and quantity, the effects of food quality or food quantity have usually been studied in isolation. In two experiments, we studied the growth and reproduction in three filter-feeding freshwater zooplankton species, i.e. Daphnia galeata x hyalina, D. pulicaria and D. magna, on their algal food (Scenedesmus obliquus), varying in carbon to phosphorus (C∶P) ratios and quantities (concentrations). In the first experiment, we found a strong positive effect of the phosphorus content of food on growth of Daphnia, both in their early and late juvenile development. Variation in the relationship between the P-content of animals and their growth rate reflected interspecific differences in nutrient requirements. Although growth rates typically decreased as development neared maturation, this did not affect these species-specific couplings between growth rate and Daphnia P-content. In the second experiment, we examined the effects of food quality on Daphnia growth at different levels of food quantity. With the same decrease in P-content of food, species with higher estimated P-content at zero growth showed a larger increase in threshold food concentrations (i.e. food concentration sufficient to meet metabolic requirements but not growth). These results suggest that physiological processes such as maintenance and growth may in combination explain effects of food quality and quantity on consumers. Our study shows that differences in response to variation in food quality and quantity exist between species. As a consequence, species-specific effects of food quality on consumer growth will also determine how species deal with varying food levels, which has implications for resource-consumer interactions.     

Potassium enrichment stimulates the growth and reproduction of a clone of Daphnia dentifera

Nutrient limitation commonly constrains organisms in natural ecosystems. Typically, ecologists focus on limitation by N and P. However, other nutrients can limit growth or reproduction. Here we focus on K limitation of invertebrate consumers (Daphnia dentifera) and phytoplankton in freshwater lakes. All organisms require K for several metabolic processes. In freshwater, K could limit growth because low external concentrations can increase the energetic costs of accumulating K. Furthermore, in a study linking K to disease, we previously found that K enrichment of water from one low-K lake stimulated the growth and reproduction of Daphnia. Here we test whether K could limit the production of Daphnia and phytoplankton across lakes and years. We repeated a life table experiment using water collected from a low-K lake during a different year. K again stimulated Daphnia reproduction. We also enriched water from 12 lakes with K or P and measured short-term growth of Daphnia and the resident algal community. Both nutrients increased Daphnia growth in five lakes. However, only P enhanced algal production. P stimulation of Daphnia positively correlated with algal quantity and the ratio of C to P in seston. However, K stimulation of Daphnia was not correlated with these factors or the background concentration of K. Thus, this study shows repeatable K-limited animal physiology in nature. Further, we can exclude the hypothesis that K stimulates Daphnia indirectly by enhancing algal production. These patterns call for future physiological studies to uncover the mechanistic basis of K limitation in natural systems.     

A note about Daphnia in Venezuelan waterbodies

After examining numerous water samples of 19 lakes and reservoirs in Venezuela, only two species of Daphnia were found: D. laevis (in colder, high altitude lakes) and D. gessneri. This observation supports the theory of the scarcity of Daphnia species in tropical inland waters.     

Role of temperature in diapause response to fish kairomones in crustacean Daphnia

The effect of non-lethal thermal conditions on the diapause response to a simulated threat of fish predation was tested in the freshwater planktonic crustacean Daphnia magna.From an early developmental stage, female Daphnia were either exposed or not exposed to fish kairomones that notified of the threat of fish predation at the benign growth temperatures of 18, 22 or 26 °C. The proportion of females switching from the production of subitaneous to diapausing eggs and their rate of reproduction were recorded.Besides the faster development and more intense reproduction observed at higher temperatures, a smaller proportion of the females formed protective, diapausing eggs when exposed to fish kairomones than was the case in colder conditions. The production of diapausing eggs was not observed when the threat of fish predation was absent. These results indicate an interactive effect of fish kairomones and thermal conditions on diapause induction in D. magna.We interpret these findings in the context of strategies for the maximisation of reproductive success. The production of well protected diapausing eggs (which assures low yet stable gains under diverse thermal conditions) may be a more beneficial life history strategy at lower temperatures, where the chances of survival of active individuals until maturation and successful reproduction are low. Higher temperatures permit faster maturation and more intensive reproduction that may surpass numerical losses of active descendants due to predation, making diapause a less rewarding option.     

Extended lifespan traded for diapause in Daphnia

1. Most freshwater crustaceans of the genus Daphnia are cyclically parthenogenetic organisms that are well adapted to unstable habitats due to their short life cycle, wide phenotypic plasticity, and the ability to produce protective diapausing eggs in anticipation of environmental deterioration. Short lifespan and heterogonic reproduction are typical features of Daphnia in a broad spectrum of freshwater habitats, from small temporary pools to large permanent lakes. However, in some locations, departures may be observed from this typical life history pattern to obligate asexuality or extended lifespan. 2. A 3‐year field study in a deep ultraoligotrophic fish‐free alpine‐type lake (Czarny Staw in the Tatra mountains in southern Poland) revealed the coexistence of two closely related asexual lineages of Daphnia of the pulex complex, which differ in body colour (transparent versus orange) and in their strategies for surviving long winters. 3. The ‘transparent’ clone of European origin exhibits an ephemeral lifestyle. It completes its life cycle within a single season, forming two generations of active specimens during the short summer and producing diapausing eggs late in the season. Transparent individuals live no longer than 5–6 months in this cold lake and survive winter exclusively in the form of diapausing eggs. 4. Individuals of the ‘orange’ lineage, which are closely related to eastern Nearctic Daphnia pulicaria, exhibit a biennial lifestyle unique to this genus. They do not form diapausing eggs or produce them only occasionally. Instead, they are active throughout the year and live for up to 13–14 months. Reproduction is postponed until the second year of life when food conditions have improved. Rich lipid reserves accumulated in the first season fuel them during the long winter and permit early reproduction the following spring. 5. Possible reasons for the evolution of obligatory parthenogenesis and long lifespan in Daphnia are discussed.     

Antibiotics affect the growth responses of <Emphasis Type="Italic">Daphnia magna</Emphasis> to poor food quality

We tested the hypothesis that exposure to antibiotics alters the growth and reproductive responses of Daphnia magna to changing stoichiometric food quality. To do so, we measured growth and reproduction of differentially P-nourished Daphnia in the presence and absence of sublethal concentrations of antibiotics. We found that exposure to an antibiotic cocktail significantly reduced an index of the microbial load of Daphnia and altered its growth responses to changing dietary P-content. Growth rates of Daphnia consuming the most P-rich and P-poor food increased with antibiotic exposure but were negatively or not affected in animals eating mildly to moderately P-limiting food. Similar effects were found in a subsequent experiment where daphnid neonates were exposed to natural bacterial communities prior to receiving antibiotics and being fed different food C:P ratios. In contrast, antibiotic effects on Daphnia reproduction were either not detected (number and size of broods) or were relatively minor (day of first reproduction). We also found no evidence that gut flora provides defense against pathogenic bacterial infection; instead, infection rates in Daphnia by a bacterial microparasite, Pasteuria ramosa, decreased in animals that had experienced prior antibiotic exposure. Our results demonstrate that antibiotic exposure reduced the microbial load and altered growth rates of an important zooplankton herbivore. Given the mediating role of animal’s food C:P ratio, our results show that interactions between Daphnia and its microbial symbionts vary in strength and nature partly with the host’s nutritional state.     

Effects of Cell-Bound Microcystins on Survival and Feeding of Daphnia spp.

The influence of cell-bound microcystins on the survival time and feeding rates of six Daphnia clones belonging to five common species was studied. To do this, the effects of the microcystin-producing Microcystis strain PCC7806 and its mutant, which has been genetically engineered to knock out microcystin synthesis, were compared. Additionally, the relationship between microcystin ingestion rate by the Daphnia clones and Daphnia survival time was analyzed. Microcystins ingested with Microcystis cells were poisonous to all Daphnia clones tested. The median survival time of the animals was closely correlated to their microcystin ingestion rate. It was therefore suggested that differences in survival among Daphnia clones were due to variations in microcystin intake rather than due to differences in susceptibility to the toxins. The correlation between median survival time and microcystin ingestion rate could be described by a reciprocal power function. Feeding experiments showed that, independent of the occurrence of microcystins, cells of wild-type PCC7806 and its mutant are able to inhibit the feeding activity of Daphnia. Both variants of PCC7806 were thus ingested at low rates. In summary, our findings strongly suggest that (i) sensitivity to the toxic effect of cell-bound microcystins is typical for Daphnia spp., (ii) Daphnia spp. and clones may have a comparable sensitivity to microcystins ingested with food particles, (iii) Daphnia spp. may be unable to distinguish between microcystin-producing and -lacking cells, and (iv) the strength of the toxic effect can be predicted from the microcystin ingestion rate of the animals.     

Longevity in Bovids Is Promoted by Sociality,But Reduced by Sexual Selection

Selection on intrinsic lifespan depends on both external factors affecting mortality and inherent tradeoffs in resource allocation between viability traits and other fitness-related traits. Longevity is therefore likely to vary between species in a sex-specific manner due to interspecific and intersexual differences in behavioural ecology. Here I focus on the bovid family to test two central hypotheses on longevity selection using the comparative method: firstly, that a reduction of extrinsic mortality in social species strengthens selection on intrinsic lifespan, and secondly, that mortality costs associated with intense sexual selection lead to shorter intrinsic lifespan. The results show that longevity (i) increases with sociality in both sexes and (ii) decreases with male-biased sexual size-dimorphism, but in males only. These discoveries suggest that sociality, a key ungulate strategy to reduce predation-related mortality, selects for inherently longer-lived organisms, and that strong sexual selection, which is known to compromise survival rates in the wild, can constrain also intrinsic lifespan. The contrasting results for males and females indicate that selection on longevity in the two sexes is partly uncoupled.     

Caenorhabditis elegans integrates food and reproductive signals in lifespan determination

Dietary restriction extends lifespan and inhibits reproduction in many species. In Caenorhabditis elegans, inhibiting reproduction by germline removal extends lifespan. Therefore, we asked whether the effect of dietary restriction on lifespan might proceed via changes in the activity of the germline. We found that dietary restriction could increase the lifespan of animals lacking the entire reproductive system. Thus, dietary restriction can extend lifespan independently of any reproductive input. However, dietary restriction produced little or no increase in the long lifespan of animals that lack germ cells. Thus, germline removal and dietary restriction may potentially activate lifespan-extending pathways that ultimately converge on the same downstream longevity mechanisms. In well-fed animals, the somatic reproductive tissues are generally completely required for germline removal to extend lifespan. We found that this was not the case in animals subjected to dietary restriction. In addition, in these animals, loss of the germline could either further lengthen lifespan or shorten lifespan, depending on the genetic background. Thus, nutrient levels play an important role in determining how the reproductive system influences longevity.