The Expensive Germline and the Evolution of Ageing

Abstract

The trade-off between survival and reproduction is the bedrock of the evolutionary theory of ageing. The reproductive system regulates ageing of the soma, and removal of germ cells extends somatic lifespan and increases resistance to a broad variety of abiotic and biotic stresses. The general explanation for this somatic response is that reduced reproduction frees up resources for survival. Remarkably, however, the disruption of molecular signaling pathways that regulate ageing increases lifespan without the obligatory reduction in fecundity, thus challenging the key role of the survival-reproduction trade-off. Here, we review the diverse literature on the costs of lifespan extension and suggest that the current paradigm is overly centered on the trade-off between lifespan and fecundity, often neglecting key aspects of fitness, such as development time, defense against parasites and, in particular, the high costs of germline maintenance. Compromised germline maintenance increases germline mutation rate, which reduces offspring fitness and ultimately can terminate germline proliferation across generations. We propose that future work should incorporate the costs of germline maintenance in the study of ageing evolution, as well as in applied biomedical research, by assessing offspring fitness.

Maternal Diet and Insulin-Like Signaling Control Intergenerational Plasticity of Progeny Size and Starvation Resistance

“…Our findings suggest an additional trade-off between progeny quantity and quality in that DR mothers produce fewer but larger progeny that cope better with early-life starvation. These observations demonstrate the importance of progeny quality as an additional metric for reproductive fitness [57]. …”

“…Reproduction is typically thought to occur at the expense of somatic maintenance and lifespan [18,57]. Using fecundity as a proxy for reproductive output simplifies analysis of this putative trade-off, but it does not fully reflect biological complexity.…”

Evolution of ageing, costs of reproduction and the fecundity–longevity trade-off in eusocial insects

“…As selection then seeks to optimize reproductive success rather than longevity, and as limited resources enforce a compromise between investment in reproduction and somatic maintenance, reproduction thereby triggers ageing and entails costs to individuals [1,2]. The result is generally, though not universally [3–6], a trade-off or negative association between fecundity and longevity [2,7]. …”

Experimentally reduced insulin/IGF-1 signaling in adulthood extends lifespan of parents and improves Darwinian fitness of their offspring

“…However, the discoveries of environmental interventions that dramatically increase healthy lifespan in model organisms without the cost of reduced reproduction have challenged the current paradigm and suggested that our understanding of the evolution of ageing is incomplete (Dillin et al. ; Kenyon ; Antebi ; Gems and Partridge ; Maklakov and Immler ; Flatt and Partridge ). Specifically, experimental downregulation of nutrient‐sensing insulin/IGF‐like (IIS) signaling pathway that governs biosynthesis in response to nutrient availability can achieve increased longevity without a concomitant decrease in reproduction in model organisms (Dillin et al.…”