Early-life reproduction predicts male lifespan in turquoise killifish (Nothobranchius furzeri)

Individuals of the same species can show striking variation in lifespan. A common assumption in life-history theory is that intra-species lifespan variation can be explained by trade-offs between reproduction and survival, i.e., individuals investing more in early-life reproduction are expected to live shorter. However, the trade-off assumption can mask alternative models. For example, individual quality could affect reproduction and survival in the same direction; e.g., high-quality individuals may both reproduce more and live longer. Here, we study the naturally short-lived turquoise killifish (Nothobranchius furzeri), an annual teleost with a limited reproductive window, which, according to the trade-off model, should generate a selective pressure that maximizes individual investment in early-life reproduction, at the expense of survival. To test the individual co-variation in reproduction and lifespan, we focused on males and performed IVFs using ejaculates collected longitudinally throughout life. Unlike the trade-off expectation, we found that reproduction outcomes of young individuals positively correlate with male lifespan, suggesting that early-life reproduction is a bona fide proxy for intrinsic individual quality. Using a causal-informed simulation, we showed that a parsimonious model where i) intrinsic quality affects both lifespan and reproduction and ii) age negatively impacts reproduction, largely recapitulates the observed data, including lifespan prediction from early-life reproduction. Our findings challenge the assumption that reproductive costs are the primary drivers of lifespan variation and instead highlight intrinsic quality as a key common cause to both lifespan and reproduction.