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

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. In this study of a recently discovered European cavefish, we provide new insights into the adaptations of subterranean organisms. Employing a large-scale common garden experiment with cave, surface, and hybrid stone loach (Barbatula barbatula ), we delve into the evolutionary drivers of phenotypic change between cave and surface forms. We demonstrate that both heritable and environmentally induced changes play a significant role in the expression of typical cave-organism traits and can facilitate rapid adaptation to subterranean environments. Our results highlight the importance of the interplay of genetics and environment in shaping species adaptation to a given habitat. The study not only sheds light on the evolution of cave organisms, it provides insights into the mechanisms and pace of evolutionary change. Relatively recently established cavefish such as the Aach cave loach are a promising candidate for understanding the nuanced processes underlying adaptation and species evolution.