Maternal senescence broadly reprograms gene expression in offspring

Abstract Offspring of older parents have reduced fitness in many species, but the mechanisms mediating this cross-generational dimension of ageing remain poorly understood. Senescence is associated with genome-wide epigenetic changes that alter transcription, raising the possibility that older parents transmit dysregulated gene expression patterns. Here we show that maternal senescence induces deleterious, transcriptome-wide reprogramming of gene expression in offspring. Gene ontology and pathway enrichment analyses reveal that broad changes in gene expression that characterise maternal senescence in the clonally reproducing arthropod Folsomia candida are also observed at a young age in the offspring of older mothers. These concordant fold-changes are apparent at the whole-transcriptome level, and encompass conserved sequalae of senescence, including reduced carbon and energy metabolism. However, senescent mothers and their offspring also exhibit some contrasting gene expression patterns, representing distinct transcriptomic signatures of senescence that are not reflected in its cross-generational effects. The broad reprogramming of gene expression in offspring of older mothers is associated with substantially reduced fitness. Our findings show that older females can transmit a senescence-like gene expression syndrome to their offspring, inducing deleterious phenotypes from a young age.