Senescence presents not only a medical problem, but also an evolutiona
ry paradox because it should be opposed by natural selection. Evolutio
nary hypotheses propose that ageing evolves as the necessary cost of p
rocesses increasing early reproductive success(1,2), or because of wea
ker selection against late-acting mutations(3). A prediction of these
hypotheses is that the rate of ageing should increase and the average
lifespan decrease as the rate of extrinsic mortality increases(1-7). A
lternatively, non-adaptive, purely mechanistic hypotheses invoke damag
e to DNA, cells, tissues and organs as being the unique cause of senes
cence and ineluctable death of organisms(8). Here we show that the evo
lution of eusociality is associated with a 100-fold increase in insect
lifespan. Such an increase is predicted by evolutionary theories beca
use termite, bee and ant queens live in colonies that are sheltered an
d heavily defended against predators. Moreover, a comparison of ants w
ith contrasting life histories also reveals an association between lif
espan and extrinsic rate of mortality. These results provide strong su
pport for evolutionary theories of ageing, as purely mechanistic hypot
heses of senescence do not propose any association between the rate of
extrinsic mortality and lifespans.