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

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.

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

“…Such combinatorial patterning modules can therefore contribute to increase pattering robustness as well as boost the potential for their evolutionary reshuffling. 33,36,37 Hence, it appears that the strict dichotomy often attributed to the deployment of these two distinct patterning concepts during embryogenesisthat is, "positional information" or "self-organization"is likely artificial and, as previously suggested, a more realistic approximation of development would entail various combinations of the two ( Figure 1B,C). 8,18,19 3 | ARTHROPOD…”

“…Collectively, combining “positional information” with growth and additional patterning modules alleviates many of the problems inherent to the establishment of highly repetitive structures, were they to be specified by “positional information” only (eg, setting up reliable long‐range gradients or precisely defining multiple threshold values). Such combinatorial patterning modules can therefore contribute to increase pattering robustness as well as boost the potential for their evolutionary reshuffling . Hence, it appears that the strict dichotomy often attributed to the deployment of these two distinct patterning concepts during embryogenesis—that is, “positional information” or “self‐organization”—is likely artificial and, as previously suggested, a more realistic approximation of development would entail various combinations of the two (Figure B,C) …”

Symmetry breaking in the embryonic skin triggers a directional and sequential front of competence during plumage patterning

“…The chicken Gallus gallus historically served as model: consistent with previous work 7 we observed that when completed (at E11) its dorsal tract covers ~77% of the skin surface and displays an orderly arrangement in which adjacent longitudinal rows (i.e., feather rows; fr) contain a reproducible number of feather follicles (F=25 as quantified between wings and tail in medial rows) and form "chevrons" along the dorso-ventral axis. For comparison, we chose two close relatives in the Galliform bird group, namely the Japanese quail Coturnix japonica and the common pheasant Phasianus colchicus in which we previously described feather distribution 17 . In Galliforms, overall tract size (~75 and 72% of dorsum surface, respectively), shape, and geometry are conserved, while the number of feathers per row is species-specific: F=17 in the quail (except in fr#1 known to develop later where F=10 17 ) and F=23 in the pheasant.…”

“…After egg incubation in Brinsea Ovaeasy 190 incubators, embryos were treated in ovo with 9mg/mL of 5-Bromo-2′-deoxyuridine solution (Sigma; BrdU incorporation experiments), and dissected. Flat skins were prepared as described previously 17 . Specimens were fixed in 4% formaldehyde, and imaged.…”

“…(b) Flat preparations of dorsal skins (left panels) and their corresponding schematic map (right panels) show that completed dorsal tracts (in pink) vary in size between the domestic chicken (where it covers ~77% of the dorsum surface; n=2), the Japanese quail C.japonica (75%; n=3), the Common pheasant P. colchicus (72%; n=3), and the zebra finch T. guttata (38%; n=2). In these four species, feather follicles (in white) organize in longitudinal rows (fr; circled numbers) that extend from the neck to the tail and contain a reproducible number of feathers F (counted from wings to tails as shown by white arrows): F=25, 10, 23, and 9 for fr#1 (in blue; note that in the Japanese quail and the zebra finch, this row is shorter as it is composed of late developing feathers10,17 ) and F=25, 17, 23, and 18, for fr#2 and fr#3 (in orange and red). In the emu D. novaehollandiae (n=3) the tract covers 100% of the dorsum surface and at E26 we quantified ~F=60 feathers along tract length).…”