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 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.

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.

The color patterns that adorn animals’ coats not only exhibit extensive diversity linked to various ecological functions but also display recurrences in geometry, orientation, or body location. How processes of pattern formation shape such phenotypic trends remains a mystery. Here, we surveyed plumage color patterns in passerine finches displaying extreme apparent variation and identified a conserved set of color domains. We linked these domains to putative embryonic skin regions instructed by early developmental tissues and outlined by the combinatory expression of few genetic markers. We found that this embryonic prepattern is largely conserved in birds displaying drastic color differences in the adult, interspecies variation resulting from the masking or display of each domain depending on their coloration. This work showed that a simple molecular landscape serves as common spatial template to extensive color pattern variation in finches, revealing that early conserved landmarks and molecular pathways are a major cause of phenotypic trends.

In extant vertebrates, natural motifs such as coat markings, spongy bone structures, neuronal arborescence or collective swarms correspond to diverse pattern types, from fractals to periodic stripes or tessellations, and so on. In this subphylum, evolution produced an apparent paradox: a given pattern may vary tremendously in its extent, periodicity or regularity, but follows general geometrical trends and is produced with meticulous precision. In this review, we discuss the role of self-organization, a patterning strategy in which spontaneous order arises through local interactions without gradient formation, in shaping both natural pattern differences and common themes. Mathematical models evidenced a wide high adaptability of self-organizing dynamics, long-advocating for their contribution to natural pattern diversity. Recent empirical and theoretical approaches taking into account network topologies and natural variation also replaced outcomes of self-organization in more constrained biological contexts, shedding light on mechanisms ensuring pattern fidelity.