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Criscuolo, F.

Publications and source records attributed to Criscuolo, F..

9 recordsLinked to original sources

Glucose and methylglyoxal alter plasma protein dynamics, immune traits and glucose homeostasis in a sex- and season-dependent manner in zebra finches

Birds maintain unusually high circulating glucose levels compared with other vertebrates without developing the diabetic complications observed in mammals, yet the mechanisms underlying this resistance remain unclear. We investigated the effects of chronic glucose and methylglyoxal supplementation on physiological condition in zebra finches (Taeniopygia guttata), with particular emphasis on sex- and season-dependent variation in plasma biochemistry, haematology and immune traits. Ninety zebra finches (45 males, 45 females) were randomly assigned to control, glucose-supplemented (50 g/L), or methylglyoxal (8.33 g/L) drinking treatments. Over one year, we analysed plasma proteins, metabolites (glucose, uric acid, bile acids), tissue damage markers (AST, CK), electrolytes, and immune parameters (leukocyte profiles). Both supplementations increased plasma glucose concentrations, with methylglyoxal producing the strongest effect. More importantly, both treatments disrupted seasonal plasma protein dynamics, preventing the increase in total proteins and globulins normally observed in females during the reproductive period, which suggests alterations in reproductive-related protein metabolism. Glucose supplementation elevated the heterophil-to-lymphocyte (H/L) ratio in May and August, consistent with elevated physiological stress. In contrast, methylglyoxal supplementation reduced the H/L ratio in November and unexpectedly lowered plasma AST and CK concentrations in May, suggesting context-dependent protective effects on tissue integrity despite its well-established pro-oxidative properties, potentially through hormetic mechanisms. Supplementation also modified the calcium/phosphate balance, further supporting treatment effects on seasonal (reproductive) physiology. Overall, our findings demonstrate that glucose and methylglyoxal reshape physiological regulation in zebra finches in a strongly sex- and season-dependent manner rather than simply inducing generalized metabolic damage. These results provide new insights into avian resistance to glucose-associated physiological challenges and highlight the importance of considering both biological context and standardized haematological reference values when investigating glucose metabolism in birds.

physiology↗

Contrasting effects of glucose and methylglyoxal supplementation on blood oxidative status, blood cells' telomere dynamics and apoptosis in birds

Birds exhibit longer lifespans than similarly sized mammals, despite having higher mass-adjusted blood glucose levels. This makes them a valuable model for the comparative study of the metabolic and physiological aspects of aging. Circulating glucose contributes to multiple pathological processes, primarily through glycation reactions and the formation of advanced glycation end-products (AGEs), as well as by promoting oxidative stress. These mechanisms are interconnected by feedback loops and play a key role in the development of age-related pathologies. To explore the causal role of glycaemia in avian ageing, we conducted a one-year dietary supplementation experiment in captive zebra finches. Birds received either glucose- or methylglyoxal-enriched water. Previously, we observed that chronic glucose supplementation in zebra finches increased mortality, an effect that did not appear to be mediated by the associated increase in plasma protein glycation or AGE levels. Therefore, the mechanisms underlying increased mortality in the glucose group remained unclear. In the present study, we investigated how glucose and methylglyoxal supplementation affect blood oxidative status and red blood cell telomere dynamics and apoptosis. We found that methylglyoxal supplementation decreased the non-enzymatic antioxidant capacity (OXY) of plasma and increased DNA damage, while glucose supplementation had no significant effect on oxidative stress, although circulating glucose levels influenced oxidative status in a sex-dependent manner. Males exhibited a positive correlation between glucose levels and organic hydroperoxides and protein carbonyls. Additionally, we report, for the first time in birds, a seasonal variation in telomere length, which was more pronounced in glucose-supplemented individuals, yet seemed independent of oxidative status. Apoptosis probability increased with both treatments, particularly with the methylglyoxal supplementation. These results highlight that glucose and methylglyoxal trigger different glucotoxicity-related pathways, with distinct effects on bird health and aging. However, the relationship between glucose supplementation and mortality remains still unclear and warrants further investigation.

physiology↗

Decoupling glycation from mortality: glucose, but not methylglyoxal, reduces survival in zebra finches

Birds provide a unique model for ageing research, with greater longevity and slower senescence compared to mammals of similar body size, despite a higher mass-adjusted metabolic rate and blood glucose levels than other vertebrate groups. While the effects of glucose, glycation, and advanced glycation end-products (AGE) on ageing are well-documented in biomedical research, their impact on avian physiology and ageing remains poorly understood. Although birds may possess adaptations mitigating the potential detrimental effects of glucose, elevated glucose still predicts reduced lifespan, and protein glycation varies with age and can influence survival and some fitness-related traits, implying that glycation or AGE accumulation may have relevant effects on avian longevity. In this study, we experimentally investigated how one year of dietary supplementation with glucose or methylglyoxal affects survival and physiology (metabolic rate, flying performance, and beak coloration) in captive zebra finches (Taeniopygia guttata). We reveal a significant increase in mortality exclusively in glucose-supplemented birds, with also an elevated albumin glycation rate and AGE formation. However, these variables did not directly explain the increased mortality, which was also absent in methylglyoxal-treated individuals, despite similar AGE accumulation. Additionally, we observed some other effects, like an age-related constraint on seasonal metabolic adjustment, a treatment-influenced age decline in secondary sexual traits expression, and a decline in flight performance during the peak mortality period, suggesting a broader deterioration of health. Thus, although we demonstrate glucose supplementation to be more deleterious than methylglyoxal, the underlying mechanisms for the increase in mortality induced by the treatment remain unresolved.

physiology↗

Glycaemia and albumin glycation rates as fitness mediators in the wild: the case of a long-lived bird

Glucose is a vital metabolic component in the functioning of organisms, but it can also bind to biomolecules through non-enzymatic glycation reactions that result in loss of functions. While the effects of glycation on health have been well demonstrated in biomedical research, little is known about the effects of glycation in wild animals. Here, we studied how plasma glucose levels and albumin glycation rates vary with age and are related to fitness in a relatively hyperglycaemic long-lived bird, the Alpine swift (Tachymarptis melba). We measured plasma glucose and albumin glycation levels before and after reproduction in adult females of known age (2-14 years), showing that, while glucose levels increased in parallel with body mass, albumin glycation rates decreased within this period. Albumin glycation, but not glucose, varies with age, peaking at 5 years, consistently with other age-related parameters previously reported in this species. Interestingly, higher plasma glucose levels before reproduction were related to increased fledging success up to a certain threshold. In addition, in terms of dynamics, females gaining more mass lowered more their glycation levels, while those gaining less mass and lowering the more their glycation levels laid more eggs. Finally, higher body mass and plasma glucose levels after reproduction predicted a higher survival probability to the next season, whereas higher albumin glycation predicted lower survival, although in an age-dependent manner. Our study highlights adult plasma glucose and glycated albumin levels as new potential markers of ageing and fitness that should be further explored in this species.

evolutionary biology↗

Understanding glycaemia and glycation levels in birds: diet and life history traits associations

The pace of life syndrome hypothesis (POLS) suggests that organisms life history, physiological and behavioural traits should co-evolve. In this framework, how glycaemia (i.e., blood glucose levels) and its reaction with proteins and other compounds (i.e. glycation) covary with life history traits remain relatively under-investigated, despite the well documented consequences of glucose and glycation on ageing, and therefore potentially on life history evolution. Birds are particularly relevant in this context given that they have the highest blood glucose levels within vertebrates and still higher mass-adjusted longevity when compared to organisms with similar physiology as mammals. We thus performed a comparative analysis on glucose and albumin glycation rates of 88 bird species from 22 orders, in relation to life history traits (body mass, clutch mass, maximum lifespan and developmental time) and diet. Glucose levels correlated positively with albumin glycation rates in a non-linear fashion, suggesting resistance to glycation in species with higher glucose levels. Plasma glucose levels decreased with increasing body mass but, contrary to what is predicted to the POLS hypothesis, glucose levels increased with maximum lifespan before reaching a plateau. Finally, terrestrial carnivores showed higher albumin glycation compared to omnivores despite not showing higher glucose, which we discuss may be related to additional factors as differential antioxidant levels or dietary composition in terms of fibres or polyunsaturated fatty acids. These results increase our knowledge about the diversity of glycaemia and glycation patterns across birds, pointing towards the existence of glycation resistance mechanisms within comparatively high glycaemic birds.

evolutionary biology↗

Mitochondrial maintenance is involved in the exceptional longevity of reproductive queens of the eusocial ant Lasius niger

Most social insects are characterized by a wide disparity in life-history traits between individuals of the same species. Sterile workers live for months or years while queens may live for decades. Theories of ageing emphasise the importance of metabolism and oxidative stress in explaining longevity, with mitochondrial bioenergetics standing at the crossroads of energy and reactive oxygen species production. Studying mitochondrial functioning therefore takes on its full relevance in determining the nature of the mechanisms that explain the contrasting longevities between insect social castes. We addressed this question in an eusocial species, the black garden ant Lasius niger. We found that caste differences in mitochondrial bioenergetics and oxidative balance only partially match with predictions of the oxidative stress theory of ageing. Long-lived queens were characterized by a lower metabolic rate, lower mitochondrial density yet not necessarily lower levels of mitochondrial oxidative damages. Despite this, queens did not show reduced ATP content; rather, they even possessed a higher energy load in their mitochondria. Converging clues suggested better mitochondrial maintenance in queen ants, with enhanced dynamics of mitochondrial fission and fusion and a more marked expression of mitochondrial enzymes of the Krebs cycle. Overall, our data paves the way for studying deeper into how the rate of ATP production per mitochondria is related to the investment in mitochondrial and somatic cellular maintenance, and whether it has specifically been selected as a key mechanism in defining the still unexplained paradoxical longevity of the queen reproductive caste.

physiology↗

Utilization of a Clark electrode device as a respirometer for small insects: a convincing test on ants allowing to detect discontinuous respiration

Respirometry provides a direct measure of an organisms respiration, which is a significant component of its metabolic rate. Amongst ants, variations in lifespan between different social castes (such as workers and queens) can be substantial, varying according to the species. As metabolic rate is higher in short-living species, we aimed to establish how metabolic rate and longevity may have coevolved within ants casts. As a first methodological step, we validate here the use of a Clark electrode initially design for measuring mitochondrial respiration control pathways, for flow-through oxygen consumption in ant, by comparison with stop flow oxygen consumption and carbon dioxide production utilizing the indirect calorimetry methodology. The global aim is to provide a reliable methodology to conduct accurate comparisons of metabolic rates within and among ant species. As expected, using Clarck electrode entails high time resolution and revealed that queens and workers exhibited discontinuous respiration, with episodes of apnea up to 20 minutes.

physiology↗

Social environment and chronological age shape eusocial insect species: the case of the ant workers.

Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly on age. As such, untangling the effects of social role and age on worker physiology is a key step towards understanding the coevolution of sociality and aging. We performed an experimental protocol that allowed a separate analysis of these two factors using four groups of black garden ant (Lasius niger) workers: young foragers, old foragers, young nest workers, and old nest workers. We highlighted age-related differences in the proteome and metabolome of workers that were primarily related to worker subcaste and only secondarily to age. The relative abundance of proteins and metabolites suggests an improved xenobiotic detoxification, and a fuel metabolism based more on lipid use than carbohydrate use in young ants, regardless of their social role. Regardless of age, proteins related to the digestive function were more abundant in nest workers than in foragers. Old foragers were mostly characterized by weak abundances of molecules with an antibiotic activity or involved in chemical communication. Finally, our results suggest that even in tiny species, extended lifespan may require to mitigate cancer risks. This is consistent with results found in eusocial rodents and thus opens up the discussion of shared mechanisms among distant taxa and the influence of sociality on life history traits such as longevity.

physiology↗

Telomere length, individual quality and fitness in female European starlings (Sturnus vulgaris) during breeding

Telomeres, short guanine-rich repeats that cap linear chromosomes, are involved in cell senescence and organismal ageing. Our present understanding of telomere function oscillates between a marker of individual quality, which should be positively correlated with reproduction, to a marker of costs of reproduction (e.g. due to DNA damage). To test these quality and cost hypotheses, we tested the output of very simple predictions in a free-living population of European starlings Sturnus vulgaris where reproductive success of adult females was followed over 2 breeding seasons (with 2 broods per breeding). If telomere length indicate individual quality, low quality females (LQ, no fledgling) should have lower telomere lengths than high quality females (which produced fledglings in 1st and 2nd broods). Additionally, physiological determinants of adult individual quality (established in a previous study) and provisioning rate should be positively associated with adult telomere lengths. Finally, telomere length should predict future reproductive success. Adult telomere length was lower in LQ females but only during the chick-rearing period. Females producing larger clutches at fledging in the 1st brood of the 1st year also had longer telomeres. Provisioning rate was positively related to telomere length, as were plasma markers of oxidative damage, non-esterified fatty acids and triglycerides. Despite these associations, we found weak support for telomeres as indicators of individual quality. Telomere length failed in predicting future reproduction success and there was a lack of consistency in within-individual telomere length over the breeding season. In starlings, we suggest that telomere length may indicate current breeding capacities and energy status of female adults, rather than future fecundity/survival.

evolutionary biology↗