Cell type diversification and phenotype convergence underlying white fin-ornamentation of cyprinid fishes

Abstract

Neural crest derived cells offer valuable opportunities to dissect mechanisms of cell fate specification and differentiation within individual ontogenies and the underpinnings of cell type diversification over evolutionary time. Particularly useful for such analyses are pigment cells of ectothermic vertebrates that arise from neural crest cells, or via latent neural crest derived stem cells, and comprise several classes with cell-type specific pigmentary phenotypes. Among these are white cells, "leucophores," present in a variety of species that contribute to patterns on the body or ornamentation on the fins. To better understand developmental and evolutionary origins of these cells we have examined leucophores harboring deposits of yellow/orange carotenoids, "xantholeucophores," of zebrafish and leucophores of white cloud minnow, within the same family Cyprinidae. We show that white phenotypes of both cell types require sepiapterin reductase that promotes accumulation of pale and colorless pteridines. We further demonstrate that xantholeucophores develop directly from yellow sepiapterin rich xanthophore-like cells and that this transition requires both gap junctional activity and permeability of the aquaglyceroporin / peroxiporin channel Aquaporin 3. These findings identify these white cells as distinct developmentally, genetically, and biochemically from another type of white cell in zebrafish and other white cells present across phylogenetic lineages. Our results highlight remarkable convergences and parallelisms in the acquisition of white cell phenotypes within and between species and identify this as a rich system for enquiries into the evolutionary individuation of novel cell types. SignificanceUnderstanding how cell types arise is fundamental to explaining animal complexity. Pigment cells offer opportunities to address this question because they display striking variation. We show that white pigment cells comprise multiple classes with independent origins. In zebrafish, white cells on one fin develop from melanophores whereas white cells on another fin develop from yellow precursors that convert their pigments to colorless ones. White cells of a related minnow require the same colorless pigments yet differ in other ways. These findings illuminate remarkable convergence: white cells have arisen repeatedly from different progenitor cell lineages by different mechanisms. This diversity--even within and between closely related species--identifies a powerful model for understanding the evolution of cell types with distinct identities and functions.