Greater Biological Repair and Maintenance in Long-Lived Ant Queens

Eusocial insects are distinguished by queens that share the same genes as the workers but that, in many species, have a far longer life span. The expression of genes associated with aging is very different in queens, something that has been observed in both ants and bees. Given this, these species can serve as a laboratory in which to gather evidence for and against a variety of hypotheses about aging, its causes, and the degree to which specific causes are important. This paper is one example among many:

Since senescence is a detrimental process with important societal and economic impacts, substantial effort has been invested into understanding its causes and many theories have been proposed to explain its origins. One of these theories proposes that senescence is caused by macromolecular damage that accumulates with age due to incomplete somatic maintenance. Lifespan is thus expected to be modulated by investment into physiological processes of damage prevention and repair. So far, investigations of somatic maintenance have mostly focused on systems of damage prevention such as anti-oxidants, and have for the most part refuted the hypothesis that longevity is achieved through damage prevention. A possible explanation for this patterns is that there is a limited potential to freely modulate the amount of reactive oxygen species because they are important signalling molecules. Such constraints are unlikely to apply to systems of macro-molecular repair, which may effectively affect lifespan by modulating the accumulation of damage with age.

Various forms of macromolecular damage have been linked to senescence. For example, DNA may be damaged or mutated in several ways, and there is evidence from mammalian studies that mutations to genes involved in DNA repair accelerate senescence. Similarly, the cellular accumulation of damaged proteins can be toxic and a range of maintenance mechanisms exist to keep this accumulation in check, many of which have been linked to ageing and longevity. One such mechanism is the Ubiquitin Proteasome System (UPS), which degrades mis-folded or damaged proteins by labelling them with ubiquitin and subsequently degrading them. Subunits of the proteasome involved in the UPS have been found to be associated with lifespan and stress resistance in a range of species, from yeast to humans.

The aim of this study is to investigate whether natural variation in lifespan is associated with differential expression of genes involved in the repair of DNA and proteins. To study the role of these somatic repair genes, we take advantage of the striking variation found in social insects, where queens and workers can differ in their lifespan by more than an order of magnitude. Importantly, the difference in lifespan must be due to differences in gene expression, since there are usually no genetic differences between castes. A particularly interesting species for studies of ageing is the ant Lasius niger, where queens can survive as long as 29 years whereas workers live for only one or two years even in laboratory conditions. Since lifespan is expected to be modulated by investment into somatic damage repair, we test the prediction that queens of L. niger have higher expression of somatic repair genes than workers.

Our analysis of 20 somatic repair genes revealed that queens and workers did not differ in their pattern of expression in 1-day-old individuals. The level of expression of these genes increased with age and this up-regulation was slightly greater in queens than in workers, resulting in significantly queen-biased expression of the 20 somatic repair genes in 2-month-old individuals in both legs and brains. Similarly, analysis of 244 genes related to DNA repair revealed no effect of caste on expression in 1-day-old individuals, but a greater up-regulation with age in queens than workers, resulting in significant queen-biased expression in the legs of 2-month-old individuals. Overall, the combination of these analyses indicates a lack of concerted differences in somatic repair gene expression between 1-day-old queens and workers, but a significantly higher level of expression in queens than workers in 2-month-old individuals.

Overall, the differences in somatic repair gene expression that we have identified between queens and workers are consistent with the hypothesis that longevity is associated with investment into somatic repair. This contrasts with results from studies investigating the process of damage prevention through anti-oxidant enzymes in social insects, where expression of antioxidant genes was found to be higher in workers than queens, perhaps to compensate for workers' the increased levels of activity. Our results suggest that damage repair may be more relevant to lifespan than removal of antioxidants. One reason for this could be the important role that antioxidants play in critical biological processes, which prevents them from being freely modulated.



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