Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish

Abstract

Colour patterns are a striking feature of animals; they evolve rapidly and play an important role in natural as well as sexual selection. It has been proposed that colour pattern formation in adult vertebrates depends on Turing-type interactions between pigment cells; however, little is known about the actual developmental mechanisms underlying the complex and prolonged ontogeny of this important adult feature. Zebrafish (Danio rerio) owe their name to a repetitive pattern of dark stripes and light interstripes parallel to the anteroposterior body axis that develop during juvenile stages. By inducible Cre/loxP-mediated recombination in neural-crest-derived progenitors, we created labelled clones of skin pigment cells that were imaged over several weeks in juvenile and adult fish. Metamorphic iridophores arise from postembryonic stem cells located at the dorsal root ganglia of the peripheral nervous system. They emerge in the skin at the horizontal myoseptum to form the first interstripe and proliferate while spreading bidirectionally along the dorsoventral axis. Patterned aggregation of iridophores during their dispersal generates a series of interstripes that define the stripe regions. Melanophore progenitors appear in situ in the presumptive stripe region where they melanize and expand in size to form compact stripes. Thus, although depending on mutual interactions between different pigment cells, stripes and interstripes are formed by a completely different cellular route.

Mathematically guided approaches to distinguish models of periodic patterning

“…In particular, we highlight a role for directed cell movement, which is important during initial patterning in juveniles (Singh et al, 2014) and during pattern regeneration (Yamaguchi et al, 2007) (Fig. 5B).…”

Response to Comment on “Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish”

“…Iridophores emerge along the horizontal myoseptum, and, after forming the first light stripe, disperse along the dorsoventral axis as a loose net of cells. Subsequently, they undergo patterned aggregation to form new light stripes (8). This spatial transition in organization prefigures the formation of dark stripes by melanophores appearing in the skin in situ; in mutants lacking iridophores, no stripes are added to a basic pattern.…”

“…2) (6, 7). Although iridophores and xanthophores have qualitatively similar interactions with melanophores, only iridophores are capable of long-range dispersal in the skin, which is important in initiating new light stripes and for the formation of a repetitive pattern (6,8). Xanthophores and melanophores only display short-scale movements during normal development (8,9).…”

“…However, experimental analyses in several organisms (4,5), including zebrafish (6)(7)(8)(9)(10), suggest these models to be oversimplifications with limited predictive value.…”

“…In the body, dark and light stripes are generated sequentially; formation of light stripes always precedes the formation of dark stripes (8). The first light-stripe region is formed following a morphological prepattern provided by the horizontal myoseptum, not by iridophores; choker mutants ( Fig.…”