Juvenile divergence in adaptive traits among seven sympatric fish ecomorphs arises before moving to different lacustrine habitats

Identifying the mechanisms initiating sympatric diversification in vertebrates has remained a conceptual challenge. Here, we analyse an assemblage of sympatric charr (Salvelinus malma) morphs from landlocked Lake Kronotskoe basin as a model to uncover the divergence pathways in freshwater fishes during the early life history stages. All morphs have distinct developmental biology, but a similar developmental rate retardation compared to the ancestor. Our study reveals that adult morphological differences, which acquire functionality at maturation, originate in the early juvenile stages due to heterochrony in skeletogenesis and allometric changes triggered by variation in metabolic activity. The craniofacial differences among the morphs result from asynchronous development of several skeletal modules. The accelerated ossification of teeth-armed bones occurs in predatory feeding morphs, whereas cranial cover ossification is promoted in benthivorous morphs. These contrasting growth patterns have led to seven phenotypes that span a range far beyond the ancestral variability. The most distinct morphs are a riverine spawning, epilimnetic predator and a lacustrine spawning, profundal benthic feeder. Taken together, we argue that the adaptive morphological differentiation in these sympatric freshwater fishes is driven by diverging patterns in ossification rate and metabolic activity against a background of uneven somatic growth. This divergence is primarily associated with basic environmental differences on the nursery grounds that might be unrelated to resource use. This nonheritable phenotype divergence is then exposed to natural selection that could result in further adaptive genetic changes.