Research Article

The periodic coloration in birds forms through a prepattern of somite origin

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Science  21 Sep 2018:
Vol. 361, Issue 6408, eaar4777
DOI: 10.1126/science.aar4777

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How birds change their stripes

From stripes to spots, animals often exhibit periodic coloration. Discrete embryonic domains (prepatterns) precede the periodic feather patterns observed in birds. After documenting natural variation in the striped pattern of galliform birds, Haupaix et al. performed long-term skin grafts to transfer the pattern of one species to another (see the Perspective by Prud'homme and Gompel). This approach revealed that periodic stripe formation obeys developmental landmarks upstream of local refining mechanisms. The somitic mesoderm first instructs stripe position through the early expression of the pigmentation gene agouti, which then controls stripe width by modulating pigment production in a dose-dependent manner. Thus, during feather patterning, a two-step process is at play.

Science, this issue p. eaar4777; see also p. 1202

Structured Abstract

INTRODUCTION

In animals, coat color is often arranged in periodic motifs that vary widely, from striped to spotted patterns. These intricate designs have long fascinated developmental biologists and mathematicians alike. What are the mechanisms underlying the formation of periodic patterns and shaping their diversity? Spatial organization in the developing skin involves prepatterns that precede the color pattern. Self-organizing events have long been thought to act upstream of prepatterns (e.g., through molecular diffusion or pigment cell interaction). Changes in both of these molecular and cellular events may contribute to periodic pattern variation. However, periodic patterns are highly reproducible within species and display specific orientation and periodicity, which suggests that they also rely on preexisting spatial reference.

RATIONALE

Documenting phenotype diversity constitutes a promising framework for the prediction of such spatial landmarks, comparable to mathematical modeling strategies. We surveyed variation in the transient periodic pattern visible in juvenile birds of the galliform group, in which longitudinal stripes are organized in a black-yellow-black sequence in the dorsal region.

RESULTS

By comparing the striped pattern for 10 galliform bird species, we showed that the width of each stripe varied and that their number increased with dorsum size. In contrast, their absolute positions were comparable. We analyzed pigment appearance in the embryonic skin of five representative species and showed that the periodic striped pattern results from the timely production of yellow coloration at specific locations. This yellow-production pulse was not triggered by a certain stage of feather growth or by dynamics of feather follicle production across the dorsum. However, it was linked to the early expression of agouti. This well-known pigmentation gene displayed a composite expression pattern in longitudinal bands whose width and position correlated with that of yellow stripes in each species. To test agouti’s role, we used a functional approach by exploiting mutant strains of quails: The increase (in the Fawn strain) or decrease (in the recessive black strain) of agouti expression levels respectively led to wider or narrower yellow stripes. Comparing pigment distribution across feathers between these gain- or loss-of-function mutants and wild-type quails showed that agouti controls stripe width by adjusting the duration of the yellow-production pulse in a dose-dependent manner. Both the position of agouti-expressing bands and that of yellow stripes did not change in mutant quails.

To identify the origin of signals controlling localized agouti expression and setting the position of yellow stripes, we performed heterospecific grafting experiments: Embryonic tissues from donor quails were transplanted into pheasant hosts. We found that after transplanting somites (from which dermal cells originate), chimeras locally displayed quail-like expression of agouti in the developing skin. Long-term experiments showed that hosts displayed a striped color pattern typical of the donor at the level of the graft. Such changes were not observed when the neural tube (from which pigment-producing cells originate) was grafted. These results showed that the somitic mesoderm autonomously instructs agouti expression and consequently the position of yellow stripes.

CONCLUSION

We conclude from this work that the galliform striped pattern is achieved in a two-step mechanism. The somite provides positional information to the developing dermis; this controls the position of agouti expression in a prepattern that foreshadows yellow stripes. Their width is then refined by agouti, which locally controls yellow production in a dose-dependent manner. This sequential organization of space, combining early landmarks and local mechanisms, may govern the formation (and thus constrain the evolution) of many periodic patterns.

The striped pattern of a Japanese quail embryo.

Galliform birds display a longitudinal pattern of colored stripes already visible a few days before hatching (here in a Japanese quail, Coturnix japonica). Stripes form through differential deposition of black and yellow pigments along growing feathers in the dorsum. Our work shows that this pattern is controlled by a prepattern instructed by the somitic mesoderm.

Abstract

The periodic stripes and spots that often adorn animals’ coats have been largely viewed as self-organizing patterns, forming through dynamics such as Turing’s reaction-diffusion within the developing skin. Whether preexisting positional information also contributes to the periodicity and orientation of these patterns has, however, remained unclear. We used natural variation in colored stripes of juvenile galliform birds to show that stripes form in a two-step process. Autonomous signaling from the somite sets stripe position by forming a composite prepattern marked by the expression profile of agouti. Subsequently, agouti regulates stripe width through dose-dependent control of local pigment production. These results reveal that early developmental landmarks can shape periodic patterns upstream of late local dynamics, and thus constrain their evolution.

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