Genetic differentiation and phenotypic plasticity drive troglomorphic character development in European cavefish

Abstract

The Aach cave loach (Barbatula barbatula), a recently discovered member of the Nemacheilidae family, offers a unique opportunity to understand the mechanisms underlying evolutionary change. In a common garden experiment, we reared groups of laboratory-bred cave, surface, and hybrid loach under different light conditions. Troglomorphic characters varied significantly among the fish, influenced to a different extent by parental origin and light conditions. Cavefish progeny consistently exhibited smaller eyes, lighter pigmentation, longer barbels, and larger olfactory epithelia than surface fish, while hybrids displayed intermediate characteristics. Surface and hybrid fish raised in complete darkness resembled the cavefish phenotype, while cavefish raised under a natural photoperiod approached the surface form. Characters associated with eye degeneration were found to be primarily heritable. Conversely, traits related to chemo- and mechano-reception were enhanced in the surface and hybrid groups reared in complete darkness, suggesting phenotypic plasticity. Our findings offer valuable insights into the interplay between genetic differentiation and phenotypic plasticity to troglomorphic adaption. This contributes to the broader understanding of the early stages of adaptation, where phenotypic plasticity, drift, and selection shape phenotypes. Relatively recently established cavefish, such as the Aach cave loach, are promising candidates for comparative research investigating evolutionary mechanisms.