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 The somite instructs a prepattern of colored stripes in galliform birds. 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. 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.

中文翻译：

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鸟类的周期性着色通过体节起源的预图案形成

鸟类如何改变条纹 从条纹到斑点，动物通常表现出周期性的着色。离散的胚胎域（预图案）先于在鸟类中观察到的周期性羽毛图案。在记录了鸡形鸟类条纹图案的自然变异后，Haupaix 等人。进行长期皮肤移植以将一个物种的模式转移到另一个物种（参见 Prud'homme 和 Gompel 的观点）。这种方法表明，周期性条纹的形成遵循局部精炼机制上游的发展标志。体节中胚层首先通过色素沉着基因 agouti 的早期表达来指示条纹位置，然后通过以剂量依赖性方式调节色素产生来控制条纹宽度。因此，在羽毛图案制作过程中，有一个两步过程在起作用。科学，这个问题 p。eaar4777; 另见第。1202 体节指示鸡形鸟类的彩色条纹预制图案。介绍 在动物中，毛色通常以周期性图案排列，这些图案变化很大，从条纹图案到斑点图案。这些复杂的设计长期以来一直让发育生物学家和数学家着迷。形成周期性模式并塑造其多样性的机制是什么？发育中的皮肤中的空间组织涉及在颜色模式之前的预制模式。长期以来，人们一直认为自组织事件在预模式的上游起作用（例如，通过分子扩散或色素细胞相互作用）。这些分子和细胞事件的变化可能导致周期性模式变化。然而，周期性模式在物种内具有高度可重复性，并显示出特定的方向和周期性，这表明它们也依赖于预先存在的空间参考。基本原理记录表型多样性构成了预测此类空间地标的有前途的框架，可与数学建模策略相媲美。我们调查了鸡形组幼鸟中可见的瞬态周期模式的变化，其中纵向条纹在背部区域以黑-黄-黑色的顺序排列。结果 通过比较 10 种鸡形鸟类的条纹图案，我们发现每个条纹的宽度各不相同，并且它们的数量随着背部尺寸的增加而增加。相比之下，他们的绝对位置是可比的。我们分析了五种代表性物种胚胎皮肤中的色素外观，并表明周期性条纹图案是由于特定位置及时产生黄色着色所致。这种产生黄色的脉冲不是由羽毛生长的某个阶段或整个背部的羽毛毛囊产生的动态触发的。然而，它与刺豚鼠的早期表达有关。这种众所周知的色素沉着基因在纵向带中显示出复合表达模式，其宽度和位置与每个物种中黄色条纹的宽度和位置相关。为了测试刺豚鼠的作用，我们通过利用鹌鹑的突变品系使用功能方法：刺豚鼠表达水平的增加（在 Fawn 品系中）或减少（在隐性黑色品系中）分别导致更宽或更窄的黄色条纹。比较这些功能获得或丧失的突变体与野生型鹌鹑羽毛上的色素分布表明，刺豚鼠通过以剂量依赖性方式调整黄色产生脉冲的持续时间来控制条纹宽度。在突变鹌鹑中，agouti 表达条带的位置和黄色条纹的位置都没有变化。为了确定控制局部刺豚鼠表达和设置黄色条纹位置的信号来源，我们进行了异种移植实验：将来自供体鹌鹑的胚胎组织移植到野鸡宿主中。我们发现在移植体节（真皮细胞的来源）后，嵌合体在发育的皮肤中局部表现出类似鹌鹑的表达。长期实验表明，宿主在移植物水平上显示出供体典型的条纹颜色图案。当移植神经管（产生色素的细胞的来源）时，没有观察到这种变化。这些结果表明体节中胚层自主指示刺豚鼠的表达，从而指示黄色条纹的位置。结论我们从这项工作中得出结论，鸡状条纹图案是通过两步机制实现的。体节为发育中的真皮提供位置信息；这在预示黄色条纹的预图案中控制了刺豚鼠表达的位置。然后它们的宽度由 agouti 细化，它以剂量依赖的方式局部控制黄色的产生。这种空间的顺序组织，结合早期地标和局部机制，可能控制许多周期性模式的形成（从而限制演化）。日本鹌鹑胚胎的条纹图案。鸡形鸟类在孵化前几天已经可以看到纵向的彩色条纹图案（这里是日本鹌鹑，Coturnix japonica）。条纹是通过黑色和黄色颜料沿着背部生长的羽毛不同沉积形成的。我们的工作表明，这种模式是由体节中胚层指示的预模式控制的。经常装饰动物皮毛的周期性条纹和斑点在很大程度上被视为自组织模式，通过动态形成，例如图灵在发育中的皮肤内的反应扩散。然而，先前存在的位置信息是否也有助于这些模式的周期性和方向，尚不清楚。我们使用雏鸡形鸟类彩色条纹的自然变化来表明条纹是在两步过程中形成的。来自体节的自主信号通过形成由刺豚鼠的表达谱标记的复合预模式来设置条纹位置。随后，刺豚鼠通过对局部色素产生的剂量依赖性控制来调节条纹宽度。这些结果表明，早期发育标志可以在晚期局部动力学上游形成周期性模式，从而限制它们的进化。刺豚鼠通过对局部色素产生的剂量依赖性控制来调节条纹宽度。这些结果表明，早期发育标志可以在晚期局部动力学上游形成周期性模式，从而限制它们的进化。刺豚鼠通过对局部色素产生的剂量依赖性控制来调节条纹宽度。这些结果表明，早期发育标志可以在晚期局部动力学上游形成周期性模式，从而限制它们的进化。