Evolutionary trade-offs between intergenerational and transgenerational fitness effects

Abstract Intergenerational and transgenerational fitness effects can shape evolutionary processes. Theoretically, however, intergenerational and transgenerational effects can trade-off with each other with profound consequences for evolutionary processes. Here we show that beneficial intergenerational effects that increase offspring fitness can result in detrimental transgenerational effects that decrease great-grand offspring fitness. We combined theoretical modelling and experimental approaches to investigate multigenerational fitness trade-offs induced by larval starvation in Caenorhabditis elegans . We demonstrate that larval starvation triggers a cascading effect: starved individuals suffered marked fitness losses, their direct offspring enjoyed fitness gains in both starvation and ad libitum environments, but great-grand-offspring paid fitness costs. Demographic simulation models revealed that genotypes exploiting this short-term intergenerational advantage outcompete rival genotypes despite the deferred transgenerational debt. Our findings demonstrate that adaptive intergenerational gains can be intrinsically linked to maladaptive transgenerational outcomes, challenging the assumption that transgenerational effects are inherently beneficial and highlighting the role of multigenerational trade-offs in evolution.