Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high-condition-dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex-specific trade-offs. Because same life-history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition-dependent mortality caused by heat shock leads to evolution of long-life, decelerated late-life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early-life and net reproduction, while mortality rate had no effect. Our results suggest that heat-shock resistance and associated long-life trade-off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.

Early-life conditions can have long-lasting effects and organisms that experience a poor start in life are often expected to age at a faster rate. Alternatively, individuals raised in high-quality environments can overinvest in early-reproduction resulting in rapid ageing. Here we use long-term experimental manipulation of early-life conditions in a natural population of collared flycatchers (Ficedula albicollis), to show that females raised in a low-competition environment have higher early-life reproduction but lower late-life reproduction than females raised in high-competition environment. We experimentally created either artificially increased (high-competition) or reduced (low-competition) broods. Reproductive success of high-competition females peaked in late-life, when low-competition females were already in steep reproductive decline and suffered from higher mortality rate. Our results demonstrate that “silver spoon” effects can increase female early-life performance at the cost of faster reproductive ageing and increased late-life mortality. These findings support the evolutionary theory of ageing and show that early-life environmental conditions shape reproductive and demographic ageing in nature.

Within-population variation in ageing remains poorly understood. In males, condition-dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early-life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high-condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low-condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High-condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male-male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early-life reproductive performance at the expense of late-life performance and survival, demonstrating a clear link between male condition and ageing.