Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in Drosophila

Reproduction and diet are two major factors controlling the physiology of
aging and life history, but how they interact to affect the evolution of
longevity is unknown. Moreover, while studies of large-effect mutants
suggest an important role of nutrient sensing pathways in regulating
aging, the genetic basis of evolutionary changes in lifespan remains
poorly understood. To address these questions, we analyzed the genomes of
experimentally evolved Drosophila melanogaster populations subjected to a
factorial combination of two selection regimes: reproductive age (early
versus postponed), and diet during the larval stage (‘low’, ‘control’,
‘high’), resulting in six treatment combinations with four replicate
populations each. Selection on reproductive age consistently affected
lifespan, with flies from the postponed reproduction regime having evolved
a longer lifespan. In contrast, larval diet affected lifespan only in
early-reproducing populations: flies adapted to the ‘low’ diet lived
longer than those adapted to control diet. Here we find genomic evidence
for strong independent evolutionary responses to either selection regime,
as well as loci that diverged in response to both regimes, thus
representing genomic interactions between the two. Overall, we find that
the genomic basis of longevity is largely independent of dietary
adaptation. Differentiated loci were not enriched for ‘canonical’
longevity genes, suggesting that naturally occurring genic targets of
selection for longevity differ qualitatively from variants found in mutant
screens. Comparing our candidate loci to those from other
‘evolve-and-resequence’ studies of longevity demonstrated significant
overlap among independent experiments. This suggests that the evolution of
longevity, despite its presumed complex and polygenic nature, might be to
some extent convergent and predictable.