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.

The development of an organism involves the formation of patterns from initially homogeneous surfaces in a reproducible manner. Simulations of various theoretical models recapitulate final states of natural patterns, yet drawing testable hypotheses from those often remains difficult. Consequently, little is known about pattern-forming events. Here, we surveyed plumage patterns and their emergence in Galliformes, ratites, passerines, and penguins, together representing the three major taxa of the avian phylogeny, and built a unified model that not only reproduces final patterns but also intrinsically generates shared and varying directionality, sequence, and duration of patterning. We used in vivo and ex vivo experiments to test its parameter-based predictions. We showed that directional and sequential pattern progression depends on a species-specific prepattern: an initial break in surface symmetry launches a travelling front of sharply defined, oriented domains with self-organising capacity. This front propagates through the timely transfer of increased cell density mediated by cell proliferation, which controls overall patterning duration. These results show that universal mechanisms combining prepatterning and self-organisation govern the timely emergence of the plumage pattern in birds.

Animals display extensive diversity in motifs adorning their coat, yet these patterns have reproducible orientation and periodicity within species or groups. Morphological variation has been traditionally used to dissect the genetic basis of evolutionary change, while pattern conservation and stability in both mathematical and organismal models has served to identify core developmental events. Two patterning theories, namely instruction and self-organisation, emerged from this work. Combined, they provide an appealing explanation for how natural patterns form and evolve, but in vivo factors underlying these mechanisms remain elusive. By bridging developmental biology and mathematics, novel frameworks recently allowed breakthroughs in our understanding of pattern establishment, unveiling how patterning strategies combine in space and time, or the importance of tissue morphogenesis in generating positional information. Adding results from surveys of natural variation to these empirical-modelling dialogues improves model inference, analysis, and in vivo testing. In this evo-devo-numerical synthesis, mathematical models have to reproduce not only given stable patterns but also the dynamics of their emergence, and the extent of inter-species variation in these dynamics through minimal parameter change. This integrative approach can help in disentangling molecular, cellular and mechanical interaction during pattern establishment.

Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling self-organized systems such that they achieve stable pattern outcomes remain unknown. Here, we described natural variation in the fidelity of self-organized arrays formed by feather follicle precursors in bird embryos. By surveying skin cells prior to and during tissue self-organization and performing species-specific ex vivo drug treatments and mechanical stress tests, we demonstrated that pattern fidelity depends on the initial amplitude of cell anisotropy in regions of the developing dermis competent to produce a pattern. Using live imaging, we showed that cell shape anisotropy is associated with a limited increase in cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which initial tissue properties ensure stability in self-organization and thus, reproducible pattern production.

SummaryCellular self-organisation can emerge from stochastic fluctuations in properties of a developing tissue1–3. This mechanism explains the production of various motifs seen in nature4–7. However, events channelling its outcomes such that patterns are produced with reproducible precision key to fitness remain unexplored. Here, we compared the dynamic emergence of feather primordia arrays in poultry, finch, emu, ostrich and penguin embryos and correlated inter-species differences in pattern fidelity to the amplitude of dermal cell anisotropy in the un-patterned tissue. Using live imaging and ex vivo perturbations in these species, we showed that cell anisotropy optimises cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which collective cellular properties of a developmental pattern system ensure stability in its self-organisation and contribute to its evolution.

The development of an organism involves the formation of patterns from initially homogeneous surfaces in a reproducible manner. Simulations of various theoretical models recapitulate final states of natural patterns 1-4 yet drawing testable hypotheses from those often remains difficult 4,5 . Consequently, little is known on pattern-forming events. Here, we extend modeling to reproduce not only the final plumage pattern of birds, but also the observed natural variation in its dynamics of emergence in five species. We built a unified model intrinsically generating the directionality, sequence, and duration of patterning, and used in vivo experiments to test its parameter-based predictions. We showed that while patterning duration is controlled by overall cell proliferation, its directional and sequential progression result from a pre-pattern: an initial break in surface symmetry launches a traveling front of increased cell density that defines domains with self-organizing capacity. These results show that universal mechanisms combining pre-patterning and self-organization govern the timely emergence of the plumage pattern in birds.