The proximate and ultimate bases of regulation of lifespan and reproduction in ants
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Abstract
Understanding why and how organisms age and die is a major topic in biology, medicine and is of universal interest. The proximate causes of aging are even less well understood than why aging evolved in the first place. One possibility is that aging results from the accumulation of molecular damage due to incomplete somatic repair. Longevity and fecundity are traded-off in most organisms and the negative association between these two traits involves conserved molecular pathways. Social insects are an exception, as fertile individuals live longer, but the mechanisms underlying this positive association are unknown. We are still far from understanding the interactions between environment, genotype, and the molecular pathways determining variation in longevity both within and between species. Social insects are ideal models, not only because they exhibit strong intra-specific variation in lifespan and reproduction with extreme values recorded in queens, but also because this variation can arise from the same genome. I investigated here the ultimate and proximate bases of the regulation of lifespan and reproduction and their reversal association in social insects, using Temnothorax ants as a study system.
I first review ultimate factors underlying variation in life-history strategies in female social insects. I highlight in chapter 1 the importance of colony size, colony founding strategy and social structure (number of queens in the colony) for the evolution of lifespan, reproduction, and body size in queens and workers. Social insects with large colony sizes and independent colony foundation exhibit the longest queen lifespans. In chapter 2, I experimentally tested the effect of colony size, body size and social structure, on egg production in ant queens. I show that colony size and social structure, but not body size, determine queen fecundity. While in most solitary insects, female body size is strongly linked to fecundity, this life-history parameter appears to be replaced by colony size in social insects.
Next, I investigated the link between fertility and somatic maintenance within castes, as well as the role of other factors for the regulation of lifespan and reproduction. By connecting phenotypic results to gene expression data, I shed light on the molecular basis of this regulation as well as the proximate mechanisms underlying the reshaping of the longevity/fecundity trade-off. In chapter 3 I investigate how longevity and fecundity are linked, and show that both egg removal and nutrient intake have a positive effect on queen fertility, but also activate body maintenance mechanisms. These results contrast with findings on solitary organisms, suggesting an alteration of molecular pathways in our species. Chapter 4 reveals that queens switch from investment into immunity to the production of antioxidants with age and increasing fertility, suggesting a role of immunity in the reversal of the longevity/fecundity trade-off. Focussing then on workers, I show in chapter 5 that behavioural castes differ in their rate of intrinsic mortality, where foragers that performed risky tasks outside the nest survive shorter than nurses. The removal of the queen induces worker fertility but also extends their lifespan. I thus investigated in chapter 6 the molecular basis of this fertility induction and lifespan extension in relation with immunity and the gut microbiome composition. I demonstrate that fertile workers upregulated repair mechanisms, explaining their extended longevity. Fertile workers respond differently to an immune challenge than non-fertile ones. Results suggest that lifespan extension is linked to a better stability of the immune response but unlikely linked to the gut microbiome.
In conclusion, this dissertation sheds light on the molecular bases of aging and the regulation of lifespan in social insects, but also reveals how social life reshapes the association of life-history traits. I bring evidence for an alteration of certain pathways in our focal social species compared to solitary ones and identify a number of candidate genes and pathways for the reshaping of the trade-off between lifespan and reproduction. Finally, I point to an important role of immunity and nutrients in the regulation of lifespan and reproduction in social insects.