The seven ways eukaryotes produce repeated colour motifs on external tissues

Abstract

The external tissues of numerous eukaryote species show repeated colour patterns, usually characterized by units that are present at least twice on the body. These dotted, striped or more complex phenotypes carry out crucial biological functions, such as partner recognition, aposematism or camouflage. Very diverse mechanisms explaining the formation of repeated colour patterns in eukaryotes have been identified and described, and it is timely to review this field from an evolutionary and developmental biology perspective. We propose a novel classification consisting of seven families of primary mechanisms: Turing(‐like), cellular automaton, multi‐induction, physical cracking, random, neuromuscular and printing. In addition, we report six pattern modifiers, acting synergistically with these primary mechanisms to enhance the spectrum of repeated colour patterns. We discuss the limitations of our classification in light of currently unexplored extant diversity. As repeated colour patterns require both the production of a repetitive structure and colouration, we also discuss the nature of the links between these two processes. A more complete understanding of the formation of repeated colour patterns in eukaryotes will require (i) a deeper exploration of biological diversity, tackling the issue of pattern elaboration during the development of non‐model taxa, and (ii) exploring some of the most promising ways to discover new families of mechanisms. Good starting points include evaluating the role of mechanisms known to produce non‐repeated colour patterns and that of mechanisms responsible for repeated spatial patterns lacking colouration.

Changing rounds into squares or combining stripes: Diversity and formation of checkerboard patterns in Eukaryotes

“…Given the periodicity of this pattern, and the round geometry of the motifs, this strongly suggests a Turing-like mechanism for its production 13 . Indeed, at that time, it is the only mechanism demonstrated to produce periodic color dots patterning in angiosperms 14 15 . Turing pattern relies classically on reaction and diffusion, and it seems that nervures could act as constraining semi-permeable barriers, which therefore shape the pattern into square-like shapes.…”

Hibiscus bullseyes reveal mechanisms controlling petal pattern proportions that influence plant-pollinator interactions

“…The suggested mechanism relies on a tug-of-war between two transcription factors from the MYB family: NEGAN (NECTAR GUIDE ANTHOCYANIN), an activator of anthocyanin pigment production 16 , and RTO (RED TONGUE), a repressor of NEGAN 11 . This model is particularly elegant as it adheres to the principle of self-organisation 32 and does not require the existence of an early pattern. In natural variants or knockout lines where RTO activity is absent, the spots are replaced by uniform pigmentation.…”

Eco-Evo-Devo of petal pigmentation patterning

“…However, pattern formation is usually tightly regulated in place and time. Thus, petals are emerging models for understanding two intimately linked developmental processes: (i) patterning, which creates regions of distinct cell types, and (ii) growth, which increases tissue size, generates organ shape and acts as a modifier of patterning processes [72,73]. During petal development, the activities of the transcription factors that regulate pigmentation pathways, cell fate specification and tissue growth are likely to be set by pre-patterns [10].…”

“…However, pattern formation is usually tightly regulated in place and time. Thus, petals are emerging models for understanding two intimately linked developmental processes: (i) patterning, which creates regions of distinct cell types, and (ii) growth, which increases tissue size, generates organ shape and acts as a modifier of patterning processes [ 72 , 73 ].…”