Stage dependent plasticity and the evolution of a non-obligate cave dwelling life cycle in frogs

Plasticity is crucial for environmental adaptation in animals, yet its role in life cycle evolution remains poorly understood. Anurans exhibit a biphasic life cycle, with tadpole and frog following distinct evolutionary trajectories. The non-obligate cave-dwelling frog Oreolalax rhodostigmatus exemplifies this phenomenon: its tadpoles have well adapted to caves, while frogs depend on outside resources. Stage-dependent adaptive plasticity may explain this paradoxical life cycle, predicting that environmental responsiveness declines after metamorphic climax and that early-stage plasticity facilitates adaptations to resource-limited cave environments.

We examined transcriptional plasticity of O. rhodostigmatus by comparing cave- and outside-dwelling tadpoles from the same population across four organs (liver, tail, skin, and hindlimb) at ten developmental stages, spanning pre-metamorphosis to metamorphic climax. Organ transcriptomes reflected both developmental and environmental effects. As predicted, transcriptional responses to environmental conditions in the liver, skin, and tail declined markedly after the onset of metamorphic climax, while the frog-specific organ, hindlimb, showed the weakest environmental responsiveness. Prior to the metamorphic climax, cave-dwelling individuals showed upregulation of fundamental cellular processes (e.g., RNA and protein synthesis) while downregulation of immune-related processes, consistent with a resource-allocation strategy in resource-limited environments. Moreover, increased expression of genes involved in bile biosynthesis and xenobiotic metabolism in the liver suggests enhanced nutrient absorption and utilization, while upregulation of glucagon- and insulin-resistance-related genes in the tail indicates improved tolerance to starvation.

Our findings support the hypothesis that stage-dependent plasticity explains the evolution of non-obligate cave-dwelling in anurans, highlighting the potential role of plasticity in shaping animal lifestyle evolution.