Abstract
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.
Highlights
IntroductionNumerous modelling studies, frequently assuming a chemical basis for pattern-forming factors (for review [1,2]) and recently integrating cellular and mechanochemical processes (for review [3,4]), led to the theorisation of self-organising dynamics to explain the emergence of many patterns
The diverse shapes and motifs that adorn animals have been a long-standing interest of theoreticians and developmental biologists: how can patterns arise from homogeneous structures during the development of an organism in an often highly organised and reproducible manner? On the one hand, numerous modelling studies, frequently assuming a chemical basis for pattern-forming factors and recently integrating cellular and mechanochemical processes, led to the theorisation of self-organising dynamics to explain the emergence of many patterns
Simulations and experimental data allow us to propose a scenario in which in Galliformes and the zebra finch, the tract becomes compartmentalised prior to the individualisation of follicular shapes in periodically arranged, oriented surfaces possessing patterning competence. These longitudinal segments appear in a medial-to-lateral travelling front triggered by a prepattern: in vivo factors are initially spatially restricted such that they create symmetry breaking in the surface field, likely constraining pattern directionality
Summary
Numerous modelling studies, frequently assuming a chemical basis for pattern-forming factors (for review [1,2]) and recently integrating cellular and mechanochemical processes (for review [3,4]), led to the theorisation of self-organising dynamics to explain the emergence of many patterns. Each of these models (both in their equations and stationary solutions) potentially describes various developmental mechanisms. Choosing and building models that accurately anticipate patterns and guide relevant tests of in vivo patterning mechanisms often remains challenging. Genetic screens and expression analyses of developmental factors—sometimes guided by modelling—have identified candidate molecules and cellular events putatively involved in pattern formation in vivo [1,2,6,7]. Biological interpretation is often limited by the difficulty to link a given pattern to prior molecular gradients and/or cell behaviours occurring in the absence of spatial reference in the a priori naïve, unpatterned tissue
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