Food, sex and death: the evolutionary biology of ageing

Chief Investigators: Rob Brooks, Russell Bonduriansky

Evolutionary research on ageing

 

Evolutionary biologists ask why organisms age (senesce), and why different species and individuals age at different rates. The major evolutionary theories of ageing are based on a crucial insight: the strength of selection inevitably declines with age because older age-classes contain fewer individuals. Ageing can then evolve for two distinct reasons. First, the Mutation Accumulation theory proposes that deleterious mutations that only affect old individuals are nearly invisible to selection, and thus accumulate in the genome, causing ageing. Second, the Antagonistic Pleiotropy theory proposes that selection favours genes that have beneficial effects in youth, but deleterious effects in old age. Ageing thus evolves as a cost of reproduction.

 

Sexually antagonistic coevolution of lifespan and ageing rate?

Differences in the ‘interests’ of females and males (i.e., sexual conflict) can affect many traits, including lifespan and ageing rate. For example, genes that reduce ageing rate may advantageous for females, but deleterious for males. It has even been suggested that males may benefit by producing toxic ejaculates, because females elevate their egg-laying rate when injured!

 

Do wild insects age?

In the protected environment of the lab, insects can live long lives and show clear signs of ageing. However, until recently, very little was known about longevity and ageing in wild insects. Using novel methods of individual marking, we obtained the first compelling evidence of ageing in a wild insect. We found that males of the little ‘antler fly’, a species that specializes on discarded antlers of moose and deer, age very rapidly: old flies exhibit elevated mortality rates and reduced reproductive rates. Moreover, we found that large males enjoy higher mating success when young, but deteriorate more rapidly with age than small males. This finding is consistent with the hypothesis that accelerated ageing occurs as a cost of high reproductive rate in youth.

 

Antler fly  mating pair (Photo: R. Bonduriansky).

We are currently investigating ageing in wild populations of the giant stilt-legged fly Telostylinus angusticollis, and the black field-cricket Teleogryllus commodus.

Marked neriid fly in the wild (Photo: R. Bonduriansky). Honours student Nori Kawasaki searching for marked flies. Marked field cricket at the Smith’s Lake Field Station (Photo: F. Zajitschek). PhD student Felix Zajitschek recapturing marked crickets near the Smith’s Lake Field Station.

Diet and ageing

Evidence from a wide range of taxa suggests that lifespan can be prolonged through a reduction in reproductive investment, or through dietary restriction. It is perhaps not surprising that one of the main hypotheses for the proximate mechanism of lifespan extension by dietary restriction is the postponement of reproduction, accompanied by reduced investment into reproductive function. However, very few studies have directly tested this hypothesis, and it is not clear how different nutrients (e.g., proteins and carbohydrates) affect lifespan. We are conducting experiments to clarify the relation between diet, reproductive effort and ageing.

 

Outdoor cricket enclosure used in reproductive ageing research at Smith’s Lake Filed Station.

Ageing research in the lab.
 

 

Sexual conflict, lifespan and ageing

It has very recently been suggested that sexually antagonistic genes may contribute to the evolution of senescence, and this idea integrates the classical models for the evolution of ageing with recent conceptual advances in evolutionary biology. We are using an experimental evolution approach by selecting populations of seed beetles under different mating and life history schedules to address these questions. We are also testing the hypothesis that sex-specific differences in inbreeding load for lifespan result from differential relationships between lifespan and fitness for males and females.

Further reading

Bonduriansky, R and Brassil, CE. 2002. Rapid and costly ageing in wild male flies. Nature 420: 377.

Bonduriansky, R and Brassil, CE. 2005. Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata). Journal of Evolutionary Biology 18: 1332-1340.

Hunt, J, Brooks, R, Jennions, MD, Smith, MJ, Bentsen, CL & Bussiere, LF. 2004. High-quality male field crickets invest heavily in sexual display but die young. Nature 432: 1024–1027.

Maklakov, AA, Kremer, N and Arnqvist, G. 2005. Adaptive male effects on female ageing in seed beetles. Proc. R. Soc. Lond. B 272: 2485–2489.

Male seed beetles have spines on their intromittent organs that puncture the female reproductive tract during the copulation. (Photo: Johanna Rönn).