Ageing can evolve by mutation accumulation and pleiotropy (trade-offs). The relative prevalence of these two mechanisms is important for determining the likelihood that mechanisms of ageing are homologous in distantly related organisms, and hence the relevance of long-lived organisms to general mechanisms of ageing. Experimental work with Drosophila, examining the properties of standing genetic variation and mutations that accumulate in real time, has provided little evidence in favour of a role for mutation accumulation, but considerable support for the importance of trade-offs, particularly between early fertility and the rate of ageing. Evidence for the roles of these two processes in the evolution of long-livedness can be derived from the response to selection, comparative studies of life history traits and testing for potential trade-offs at the mechanistic level.