Differential growth is a critical determinant of zebrafish pigment pattern formation

Abstract

The skin patterns of vertebrates are formed by complex interactions between pigment-producing cells during development. Adult zebrafish (Danio rerio), a model organism for investigating the underlying patterning processes, display alternating horizontal blue and golden stripes, generated by the self-organisation of three pigment cell-types. Mathematical studies in which these cells are modelled as individual agents communicating via short- and long-range interactions have produced breakthroughs in the understanding of pattern development. These models, incorporating all experimentally evidenced cell-cell interactions, replicate many aspects of wild-type and mutant zebrafish patterns. Although received wisdom suggested that initial iridophore distribution was pivotal in orienting patterning, here we show that growth can override its influence. Altered growth sequences can generate further pattern modulation, including vertical stripes and maze-like patterns. We demonstrate that ventrally-biased (asymmetric) growth of the skin field explains two key zebrafish pattern development features which are otherwise obscure (dorso-ventral pattern asymmetry, and predominant ventral-to-dorsal migration of melanophores) in wild-type and multiple zebrafish mutants, and in the related species Danio nigrofasciatus. By identifying biased growth as a novel patterning mechanism, our study will inform future investigations into the mechanisms and evolution of fish pigment patterning and vertebrate pigment pattern formation. Furthermore, our work has implications for the mechanistic basis of human pigmentation defects.

Mechanochemical Principles of Spatial and Temporal Patterns in Cells and Tissues

“…However, it was later shown that the interactions between the pigment cells were regulated by cell projections instead of diffusion (Eom et al 2015;Mahalwar et al 2014) and that therefore, while the criteria for local activation and long-range inhibition still held, it did not fit the traditional reaction-diffusion requirements of a true Turing pattern (Watanabe & Kondo 2015a,b). Even more recently, it has been suggested that growth of the tissue is important for stripe formation as well (Owen et al 2021). This pattern could thus be said to be formed by a 'Turing-like' mechanism, where cell motion takes the role of molecular diffusion in the original Turing mathematical model.…”