Phenotypic plasticity and genetic differentiation drive troglomorphic character development in European cave loach

Abstract

Using a cross-fostering experiment, we provide evidence for the contribution of both genetic differentiation and phenotypic plasticity to troglomorphic character development in the recently discovered cave form of Barbatula barbatula, an evolutionarily young lineage and first cavefish described in Europe, the northernmost record. We established reproducing populations of cave- and surface-dwelling loaches to produce cave, surface, and hybrid offspring and reared the F1 fish in a common garden setting in total darkness (DD) to simulate cave conditions as well as under the natural photoperiod (DL). We observed significant differences in the occurrence and extent of typical troglomorphic target characters among the offspring groups. Regardless of rearing conditions, cave fish exhibited smaller eyes, lighter body coloration, longer barbels, and larger olfactory epithelium than seen in surface fish. Hybrids in both rearing conditions generally showed an intermediate level of these traits. Surface and hybrid DD fish differed from the DL groups, resembling the cave fish phenotype in several traits, including eye size and body pigmentation. In contrast, cave and hybrid DL fish groups resembled surface fish phenotypes. Results confirmed that troglomorphic traits arise from heritable genetic differentiation of cave from surface forms and that phenotypic plasticity contributes to the process of adaptation to novel light conditions.