1. Ecology
  2. Evolutionary Biology

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

  1. Adrián Moreno Borrallo  Is a corresponding author
  2. Sarahi Jaramillo Ortiz
  3. Christine Schaeffer-Reiss
  4. Benoît Quintard
  5. Benjamin Rey
  6. Pierre Bize
  7. Vincent A Viblanc
  8. Thierry Boulinier
  9. Olivier Chastel
  10. Jorge S Gutiérrez
  11. José A Masero
  12. Fabrice Bertile
  13. Francois Criscuolo
  1. University of Strasbourg, CNRS, Institut Pluridisciplinaire Hubert Curien, France
  2. National Proteomics Infrastructure, ProFi, France
  3. Parc Zoologique et Botanique de Mulhouse, France
  4. Lyon University 1, UMR CNRS 5558, Laboratoire de Biométrie et Biologie Evolutive, France
  5. Swiss Ornithological Institute, Switzerland
  6. CEFE, Montpellier University, CNRS, EPHE, IRD, France
  7. Center of Biological Studies of Chizé (CEBC), UMR 7372 CNRS - La Rochelle University, France
  8. Ecology in the Anthropocene, Associated Unit CSIC‑UEX, Faculty of Sciences, University of Extremadura, Spain
https://doi.org/10.7554/eLife.103205.4
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Cite this article
  1. Adrián Moreno Borrallo
  2. Sarahi Jaramillo Ortiz
  3. Christine Schaeffer-Reiss
  4. Benoît Quintard
  5. Benjamin Rey
  6. Pierre Bize
  7. Vincent A Viblanc
  8. Thierry Boulinier
  9. Olivier Chastel
  10. Jorge S Gutiérrez
  11. José A Masero
  12. Fabrice Bertile
  13. Francois Criscuolo
(2025)
Variation in albumin glycation rates in birds suggests resistance to relative hyperglycaemia rather than conformity to the pace of life syndrome hypothesis
eLife 13:RP103205.
https://doi.org/10.7554/eLife.103205.4
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4 figures, 4 tables and 7 additional files

Figures

Figure 1
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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
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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
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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], pMCMC = 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
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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).

Tables

Table 1
Final glucose model with diet, body mass, life history traits, and sample provenance (wild versus captive; see Appendix 1) as explanatory variables, including the significant quadratic effect of maximum lifespan.

Posterior means, CI95 and pMCMC from a phylogenetic MCMC GLMM model including n = 326 individuals of 58 species.Both glucose and body mass are log10 transformed and life history traits are residuals from a phylogenetically controlled generalized least-squares model (pGLS) model of log10 body mass and log10 of the trait in question (see Appendix 1). Body mass was also centred to better explain the intercept, as 0 body mass would make no biological sense. The intercept corresponds to the omnivore diet, being used as the reference as it is considered the most diverse and ‘neutral’ group for this purpose. Significant predictors are indicated in bold.

EstimatesLower 95% CIUpper 95% CISampling effortpMCMC
Intercept (omnivore)2.3872.2682.559,900<0.001
Diet: carnivore terrestrial0.02–0.0560.09959,9000.592
Diet: aquatic predator0.034–0.0470.11259,9000.393
Diet: herbivore–0.053–0.1770.0759,9000.393
Diet: frugivore/granivore–0.055–0.2390.13559,9000.558
Centred Log10 body mass–0.061–0.106–0.01559,9000.009
Maximum lifespan0.107–0.0350.25359,9000.142
Maximum lifespan2–0.616–1.166–0.09559,9000.026
Clutch mass–0.095–0.2650.06959,9000.258
Developmental time0.011–0.1850.21259,9000.916
Provenance: captive0.034–0.0390.10659,9000.346
Table 2
Final glycation model with diet, body mass, glucose, and life history traits as explanatory variables.

Posterior means, CI95, and pMCMC from a phylogenetic MCMC GLMM model including n = 316 individuals of 58 species.Glycation, glucose, and body mass are log10 transformed and life history traits are residuals from a linear model of log10 body mass and log10 of the trait in question (see Appendix 1). Body mass and glucose were also centred to better explain the intercept. The intercept corresponds to the omnivore diet, being used as the reference as it is considered the most diverse and ‘neutral’ group for this purpose. Significant predictors are indicated in bold, and the credible intervals are considered for making pairwise comparisons between the groups.

EstimatesLower 95% CIUpper 95% CISampling effortpMCMC
Intercept1.2321.1121.35159,900<0.001
Diet: carnivore terrestrial0.1010.0170.18759,9000.021
Diet: aquatic predator0.027–0.0620.11859,9000.549
Diet: herbivore–0.019–0.1610.11959,9360.781
Diet: frugivore/granivore0.095–0.0980.29259,9000.329
Centred log10 body mass0.004–0.0430.0558,7650.876
Log10 glucose0.1370.0120.25559,9000.027
Maximum lifespan0.037–0.1220.19559,0430.648
Clutch mass0.151–0.030.34659,9000.114
Developmental time0.04–0.1880.26659,3030.725
Appendix 1—table 1
Main set of models performed with the number of species and individuals included in them.

A total of 10 MCMCglmm models were performed, having either plasma glucose or albumin glycation levels as response variable and a different number of species and total datapoints depending on if the life history (LH) traits were included (i.e. maximum lifespan, clutch mass, and developmental time) or only diet and body mass (also glucose in the glycation models). The models considering age and 201 sex did not include life history traits nor diet.

Models performed and N for eachSpecies averagesIntraspecific variationAge and sex
GlucoseGlycationGlucoseGlycationGlucoseGlycation
Non- LHLHNon- LHLHNon- LHLHNon- LHLH
Number of species88668866755875584949
Number of individuals379316379316239239
Appendix 1—table 2
List of species used in the models testing the relationship between the number of albumin’s exposed lysines and its glycation rates.

On the left, the list of considered species and on the right, the list of species used as references for the number of exposed lysines. The ones in bold are those that coincide.

Species in our datasetOriginal species
Anas platyrhynchosAnas platyrhynchos
Anser anserAnser brachyrhynchus*
Anser indicusAnser cygnoides*
Aptenodytes patagonicusAptenodytes patagonicus
Tachimarptos melbaApus apus
Aythya baeriAythya fuligula
Balearica regulorumBalearica regulorum
Bubo buboBubo bubo
Cariama cristataCariama cristata
Cygnus atratusCygnus atratus
Eudyptes chrysolophusEudyptes chrysolophus
Limosa limosaLimosa lapponica
Numida meleagrisNumida meleagris
Leucocarbo verrucosusPhalacrocorax carbo
Phoenicopterus ruberPhoenicopterus ruber
Pygoscelis papuaPygoscelis papua
Rhea pennataRhea pennata
Taeniopygia guttataTaeniopygia guttata
Tauraco erythrolophusTauraco erythrolophus
Turdus merulaTurdus rufiventris
  1. *

    For these species, as they both belong to the same genus, an average was calculated for both the number of exposed lysines and the glycation levels, considering them in the analyses as one. This way, Aser anser and Anser indicus were substituted by an Anser sp. average glycation value, and Anser brachyrhynchus and Anser cygnoides by an average number of lysine exposed. The actual values were very similar in both cases, so this average is likely to reflect realistic values.

Additional files

MDAR checklist
https://cdn.elifesciences.org/articles/103205/elife-103205-mdarchecklist1-v1.pdf
Supplementary file 1

Detailed models' outcomes.

https://cdn.elifesciences.org/articles/103205/elife-103205-supp1-v1.pdf
Supplementary file 2

Additional figures.

https://cdn.elifesciences.org/articles/103205/elife-103205-supp2-v1.pdf
Supplementary file 3

Provenance of the samples.

https://cdn.elifesciences.org/articles/103205/elife-103205-supp3-v1.xlsx
Supplementary file 4

References for the data values used as quoted in the dataset (Supplementary file 5).

https://cdn.elifesciences.org/articles/103205/elife-103205-supp4-v1.pdf
Supplementary file 5

Dataset.

https://cdn.elifesciences.org/articles/103205/elife-103205-supp5-v1.xlsx
Supplementary file 6

Code.

https://cdn.elifesciences.org/articles/103205/elife-103205-supp6-v1.r

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  1. Adrián Moreno Borrallo
  2. Sarahi Jaramillo Ortiz
  3. Christine Schaeffer-Reiss
  4. Benoît Quintard
  5. Benjamin Rey
  6. Pierre Bize
  7. Vincent A Viblanc
  8. Thierry Boulinier
  9. Olivier Chastel
  10. Jorge S Gutiérrez
  11. José A Masero
  12. Fabrice Bertile
  13. Francois Criscuolo
(2025)
Variation in albumin glycation rates in birds suggests resistance to relative hyperglycaemia rather than conformity to the pace of life syndrome hypothesis
eLife 13:RP103205.
https://doi.org/10.7554/eLife.103205.4