Long-term effects of the early life environment on alternative splicing

All organisms respond to their environments, and early life environments may be especially impactful. Alternative splicing has been implicated as one mechanism that may underlie the response of organisms to their environments. However, most studies of this type examine immediate effects of an environmental perturbation on patterns of alternative splicing; little is known about the long-term consequences of early life environments. Here, we show the early life environment exerts a lasting influence on patterns of alternative splicing in the pea aphid (Acyrthosiphon pisum). This species is sensitive to conspecific density (crowding), with a transgenerational (mother-to-daughter) wing polyphenism cued by this environmental signal. We demonstrate that the maternal environment during embryonic development alters daughters alternative splicing profiles independently of morph identity, and that these effects persist into adulthood. By comparing the magnitude of maternal-environment effects to morph-specific differences, we reveal that the influence of early environmental conditions on splicing is unexpectedly large. These findings suggest that environmental history can leave a persistent molecular imprint beyond its role in morph determination. More broadly, this work highlights the need to disentangle environmental and morph-specific transcriptomic variation in studies of developmental polyphenism and connects to broader efforts, across biology and medicine, to understand how early life experiences shape long-term molecular and physiological outcomes.