Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution

Abstract

Fishes have diverse pigment patterns, yet mechanisms of pattern evolution remain poorly understood. In zebrafish, Danio rerio, pigment-cell autonomous interactions generate dark stripes of melanophores that alternate with light interstripes of xanthophores and iridophores. Here, we identify mechanisms underlying the evolution of a uniform pattern in D. albolineatus in which all three pigment cell classes are intermingled. We show that in this species xanthophores differentiate precociously over a wider area, and that cis regulatory evolution has increased expression of xanthogenic Colony Stimulating Factor-1 (Csf1). Expressing Csf1 similarly in D. rerio has cascading effects, driving the intermingling of all three pigment cell classes and resulting in the loss of stripes, as in D. albolineatus. Our results identify novel mechanisms of pattern development and illustrate how pattern diversity can be generated when a core network of pigment-cell autonomous interactions is coupled with changes in pigment cell differentiation.

Modelling stripe formation in zebrafish: an agent-based approach

“…It has also been observed [23] that iridophores may have a role in bounding stripe width, and, in support of this empirical observation [23], we find that melanophores are more widely dispersed across the fish skin when additional iridophores are not introduced. Furthermore, our results suggest that some delay in the appearance of additional alignment information is important to preserve the sequential nature of stripe pattern formation.…”

“…Frohnhö fer et al [4] have suggested that attractive interactions between xanthophores and the dense S-iridophores underneath them may be responsible for confining interstripes. Furthermore, Patterson et al [23] demonstrated that overexpression of xanthophores and reduction in iridophores on the fish skin is linked to intermingling of cells at stripe/interstripe boundaries. Thus, it appears that interactions between all three types of pigment cells may be involved in preserving the sharp separation between melanophores and xanthophores (for proposed networks of such interactions, see [4,26]).…”

“…By conducting iridophore ablation experiments, Parichy and his laboratory [23,26] have also shown that iridophores play an active organizational role in specifying stripe/interstripe Pattern generated 100 days after simulation began under mechanism B; xanthophores migrate towards stripes, disrupting alignment. The initial condition used for both images is a set of adult stripes and interstripes with cells at the experimentally measured distances [16] apart (see §3.5.2).…”

“…Instead, we take an indirect route based on empirical observations [23,26] that iridophores promote and instruct the placement of xanthophores. In particular, we model this effect of delayed iridophore localization by introducing two narrow (one cell wide) strips of xanthophores at 20% and 80% of the current fish domain height at a delayed time.…”

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

“…Xanthophores and melanophores only display short-scale movements during normal development (8,9). This has recently been supported by an independent study indicating that iridophores regulate melanophore stripe position and width (13). However, the current Turingmodel does not consider iridophores.…”