ABSTRACT
Subterranean habitats offer excellent opportunities to understand how adaptive phenotypes originate in changing environments. Cave dwelling animals show a suite of specialized traits associated with survival in a highly specialized dark environment. A widely accepted model for the evolution of cave animals posits cave colonization by surface dwelling ancestors followed by the acquisition of adaptive traits by standing genetic variation or new mutations over many generations. However, the speed of cave adaptation in some species is difficult to reconcile with this conventional viewpoint, suggesting the importance of alternative mechanisms operating over shorter timescales. To address these mechanisms, we exposed Astyanax mexicanus surface fish (SF) to completely dark (D/D) conditions during early development and compared them to siblings placed on a standard photoperiod (L/D). We identified multiple traits that were altered in D/D SF compared to L/D SF adults raised in complete darkness for up to 2 years. On a transcriptome level, these changes included differences in the expression of 356 genes related to sensory systems, endocrine signaling, circadian rhythms, the blood, and numerous metabolic changes, especially in lipids. On a phenotypic level, we found alterations in eye anatomy, pigmentation, metabolic rates, starvation resistance, hormone levels, and neurotransmitter levels. Remarkably, most of these alterations are associated with known adaptations to the cave environment that change in the direction of the cavefish phenotype. Contrary to the widely accepted view that cave-related traits result from long-term genetic processes, our results indicate that some traits can appear within a single generation by phenotypic plasticity. We also show that plasticity is a developmental and evolvable trait and that the initial plastic responses are random in terms of their adaptive outcome but may determine the subsequent course of adaptive evolution. Our study suggests that phenotypic plasticity may significantly contribute to the rapid evolution of cave-related traits providing a foundation for genetic assimilation in colonization of A. mexicanus to dark cave environments.
