Abstract
The relationship between brain size and ageing is a paradox. The cognitive benefits of large brains should protect from extrinsic mortality and thus indirectly select for slower ageing. However, the substantial energetic cost of neural tissue may also impact the energetic budget of large-brained organisms, causing less investment in somatic maintenance and thereby faster ageing. While the positive association between brain size and survival in the wild is well established, no studies exist on the direct effects of brain size on ageing. Here we test how brain size influences intrinsic ageing in guppy (Poecilia reticulata) brain size selection lines with 12% difference in relative brain size. Measuring survival under benign conditions, we find that large-brained animals live 22% shorter than small-brained animals and the effect is similar in both males and females. Our results suggest a trade-off between investment into brain size and somatic maintenance. This implies that the link between brain size and ageing is contingent on the mechanism of mortality, and selection for positive correlations between brain size and ageing should occur mainly under cognition-driven survival benefits from increased brain size. We show that accelerated ageing can be a cost of evolving a larger brain.
Highlights
A long life can be achieved by minimizing extrinsic causes of death and/or decelerating intrinsic ageing
As large brains can mediate a decrease in extrinsic mortality and experimentally changing extrinsic mortality often drives the evolution of ageing rates [9,10,11], evolving larger brains may be evolutionarily correlated with slower ageing
While males and females did not differ in lifespan, small-brained animals survived on average 22% longer than large-brained animals (Cox regression: brain size selection regime: z 1⁄4 2.78, p 1⁄4 0.005, sex: z 1⁄4 0.13, p 1⁄4 0.900; table 1 and figure 1a)
Summary
A long life can be achieved by minimizing extrinsic causes of death and/or decelerating intrinsic ageing. The present ambiguity over the mechanisms that affect the correlation between brain size and ageing means that further analysis is important to fully understand this link This is the case for the question of how intrinsic ageing is affected by brain size under conditions limiting correlated selection, where no empirical data are presently available. We kept males and females of three large- and three small-brained selection lines, which differ by 12% in relative brain size [3], under near ad libitum food availability in individual tanks and determined their lifespan. We examined the relationship between brain size and intrinsic longevity in lines of Trinidadian guppies that were artificially selected for large or small relative brain size [18]. The analysis was done using the ‘coxme’ package in R [20]
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