Variation in albumin glycation rates in birds suggests resistance to relative hyperglycaemia rather than conformity to the pace of life syndrome hypothesis

Abstract

The pace of life syndrome (POLS) hypothesis suggests that organisms' life history and 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 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 in 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.

Keywords: birds; comparative method; ecology; evolutionary biology; glucose; glycation; life-history; longevity.

Figure 1.. Average plasma glucose values in mg/dL (in grey) and average albumin glycation rate as a percentage of total albumin (in blue) from all the species used in this study (some of them with glucose values coming from ZIMs database; see ‘Materials and methods’) with the orders they belong to.

Glucose and glycation values are standardized in order to be compared, with the dotted lines representing half the maximum and maximum values for each variable (as indicated by the axes in their corresponding colours), from inside out. Tree from a consensus on 10,000 trees obtained from ‘Hackett All species’ on Birdtree.org, including 88 species from 22 orders (see ‘Materials and methods).

Figure 2.. Plasma glucose levels (in mg/dL) variation as a function of (A) species mean-centred body mass and (B) residual maximum lifespan.

Both glucose and body mass are log transformed. Maximum lifespan (in years) is given as the residues of a phylogenetically controlled generalized least-squares model (pGLS) model with body mass (in grams), both log₁₀ transformed, so the effects of body mass on longevity are factored out (see Appendix 1). Different bird orders, are indicated by symbols, as specified on the legends at the right side of the graphs. (A) uses the values and estimates from the glucose model without life history traits (n = 389 individuals from 75 species), while (B) uses only the data points employed on the complete model (n = 326 individuals of 58 species).

Figure 3.. Outcomes of the models (estimates with interquartile ranges from the posterior distributions and whiskers representing credible intervals) on individual data on effects of diet on (A) plasma glucose levels and (B) albumin glycation in birds.

Glucose levels are given in mg/dL, while glycation levels are a percentage of total plasma albumin which is found to be glycated. Terrestrial carnivores showed significantly higher glycation levels than omnivores (estimate = 21.62 %, CI₉₅[18, 25.95], p_MCMC = 0.049). Models without life history traits, including more individuals, are represented, but the models with life history traits do not show differences in their qualitative predictions (i.e. higher albumin glycation in terrestrial carnivores than in omnivores; see Supplementary file 1).

Figure 4.. Individual albumin glycation rates (as a percentage of total albumin) variation as a function of individual plasma glucose values (mg/dL).

(A) Both variables log₁₀ transformed, as in the model, including the line representing the predicted relationship. (B) Both variables in a linear form, to more explicitly illustrate the phenomenon referred to as higher albumin glycation resistance in birds with higher plasma glucose levels, inferred from the faster increase in glucose than albumin glycation, that is, the negative curvature of the relationship. Different bird orders are indicated by symbols, as specified on the legends at the right side of the graphs. The values and estimates used are from the glycation model without life history traits (n = 379 individuals from 75 species).