Oxidative stress and senescence in social insects: a significant but inconsistent link?

Abstract

The life-prolonging effects of antioxidants have long entered popular culture, but the scientific community still debates whether free radicals and the resulting oxidative stress negatively affect longevity. Social insects are intriguing models for analysing the relationship between oxidative stress and senescence because life histories differ vastly between long-lived reproductives and the genetically similar but short-lived workers. Here, we present the results of an experiment on the accumulation of oxidative damage to proteins, and a comparative analysis of the expression of 20 selected genes commonly involved in managing oxidative damage, across four species of social insects: a termite, two bees and an ant. Although the source of analysed tissue varied across the four species, our results suggest that oxidative stress is a significant factor in senescence and that its manifestation and antioxidant defenses differ among species, making it difficult to find general patterns. More detailed and controlled investigations on why responses to oxidative stress may differ across social species may lead to a better understanding of the relations between oxidative stress, antioxidants, social life history and senescence. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Keywords: ageing; antioxidant genes; longevity; protein oxidation; social insects; transcriptomes.

Figure 1.

Quantification of carbonyl groups (DNPH assay) in oxidized proteins. (a) The phylogeny and the silhouettes of the species tested. (b–g) The quantification of carbonyl groups (in nmol carbonyl/mg protein) for young and old reproductive individuals of (b) the termite Cryptotermes secundus (n = 7 for each group) and (c) the bee Euglossa viridissima (solitary young/old: n = 4/5, queen young/old: n = 4/7) and for young and old non-reproductive individuals of (d) C. secundus (workers young/old: n = 7/7), (e) E. viridissima (workers young/old: n = 5/3), (f) the bee Apis mellifera (workers young/old: n = 12/9) and (g) the ant Platythyrea punctata (workers young/old: n = 9/9). E. viridissima is a facultative eusocial bee species; therefore, we distinguished between solitary and social nest structures for reproductive individuals. The boxplots represent the median (bold line), the lower and upper boundaries of the boxes correspond, respectively, to the 25th and 75th percentiles. Each point represents the original datum of one individual. Results of the statistical analysis are shown in table 1 and electronic supplementary material, Methods S1.

Figure 2.

Results of principal component analyses (PCAs) based on the expression of the 20 candidate antioxidant genes common to the four species studied and presented by species: (a) the ant Platythyrea punctata (abdomen), (b) the termite Cryptotermes secundus (whole body without guts), and the bees (c) Apis mellifera capensis (fat body of pseudoqueens and workers and (d) Euglossa viridissima (abdomen). Shown are the first (abscissa) and second (ordinate) principal components (PC) with variance explained by each PC. Each point represents the expression profile of one individual. Yellow shapes represent young and brown shapes old individuals, triangles represent reproductive individuals and circles, non-reproductive individuals. The ellipses displayed on the PCA plots highlight the main results of the PERMANOVA for each species (see main text), yellow/brown ellipses indicate an age effect, while black ellipses indicate a caste effect.

Figure 3.

Results of principal component analyses (PCAs) based on the expression of the 20 selected candidate antioxidant genes across four species studied (Platythyrea punctata, Cryptotermes secundus, Apis mellifera capensis, Euglossa viridissima). Shown are the first (abscissa) and second (ordinate) principal components (PC) with variance explained by each PC. Each point represents the expression profile of one individual. Yellow shapes represent young and brown shapes old individuals, triangles represent reproductive individuals and circles, non-reproductive individuals. The ellipses (95% confidence interval) displayed on the PCA plots highlight the variable ‘species'. Note that samples of both tissues (head and abdomen) are included for Platythyrea punctata.