A quantitative modelling approach to zebrafish pigment pattern formation.

Jennifer P Owen,Christian A Yates,Robert N Kelsh

doi:10.7554/elife.52998

Abstract

Pattern formation is a key aspect of development. Adult zebrafish exhibit a striking striped pattern generated through the self-organisation of three different chromatophores. Numerous investigations have revealed a multitude of individual cell-cell interactions important for this self-organisation, but it has remained unclear whether these known biological rules were sufficient to explain pattern formation. To test this, we present an individual-based mathematical model incorporating all the important cell-types and known interactions. The model qualitatively and quantitatively reproduces wild type and mutant pigment pattern development. We use it to resolve a number of outstanding biological uncertainties, including the roles of domain growth and the initial iridophore stripe, and to generate hypotheses about the functions of leopard. We conclude that our rule-set is sufficient to recapitulate wild-type and mutant patterns. Our work now leads the way for further in silico exploration of the developmental and evolutionary implications of this pigment patterning system.

Highlights

Pattern formation - the process generating regular features from homogeneity - is a fascinating phenomenon that is as ubiquitous as it is diverse
Unlike previous models of stripe formation (Nakamasu et al, 2009; Bullara and De Decker, 2015; Volkening and Sandstede, 2015; Painter et al, 2015; Bloomfield et al, 2011; Volkening and Sandstede, 2018), we include xanthoblasts as an independent cell-type in our model. This is because the larval xanthoblasts appear principally by dedifferentiation of the embryonic xanthophores, and most metamorphic xanthophores arise from the larval xanthoblasts (Mahalwar et al, 2014; McMenamin et al, 2014; Budi et al, 2011; Singh et al, 2014; Dooley et al, 2013), whilst xanthoblasts that do not re-differentiate into xanthophores persist in the stripe regions where they play a role in consolidating melanocytes into stripes
We propose that dense S-iridophores are attracted in the short range to xanthophores since they are highly associated with each other in each of the mutants and in wild type (WT) (Frohnhofer et al, 2013), and this mutual attraction may be important for interstripe consolidation

Summary

Introduction

Pattern formation - the process generating regular features from homogeneity - is a fascinating phenomenon that is as ubiquitous as it is diverse It is a major aspect of developmental biology, with key exemplars including segmentation within the syncitial blastoderm of fruit flies (Clark and Peel, 2018), digit formation in the vertebrate limb (Tickle, 2006), and branching patterns in kidney and lung development (Davies, 2002). They form rapidly and, in many cases, autonomously, that is, the process relies on self-organisation and not internal body structures. They often vary dramatically between even closely related species, recognising similarities and differences in the development of these related species can allow us insight into the evolutionary change. Pigment pattern formation is made experimentally tractable by the self-labelling nature of pigment cells

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