Morphological and Physiological Colour Changes in the Animal Kingdom

Abstract

Colour change is the ability of an organism to modify its colouration in response to specific stimuli. Several biological functions have been proposed to explain colour changes, including ultraviolet (UV) protection, thermoregulation, crypsis, inter‐ and intraspecific communication. Changes in body colouration are mainly performed through two types of mechanisms referred to as morphological and physiological. Mechanistically, these two types of colour changes differ in their speed and the way coloured structures are altered. The proximal causes of these colour changes are identified in a handful number of species and demonstrate that common physiological, cellular and molecular actors are at play. However, the reasons why both colour‐change types are widespread in the animal kingdom and how they have evolved are still unknown. This is partly due to a lack of knowledge about the fitness implications of colour changes, particularly their energetic costs.

Key Concepts

  • Morphological and physiological colour changes are widespread in the animal kingdom.
  • It has been suggested that both types of colour changes have the same biological functions, which are UV protection, thermoregulation, crypsis, inter‐ and intraspecific communication.
  • Despite differences in speed and mechanisms, similar cellular and molecular actors are at play for both types of colour changes.
  • Colour changes are triggered by environmental stimuli, mainly light, and are regulated by the neuronal and hormonal systems.
  • The evolution of colour‐changing abilities is still poorly understood because the consequences of colour changes on individual fitness remain to be investigated.

Keywords: colour changing; morphological colour changes; physiological colour changes; animal evolution; pigment; chromatophore; camouflage; melanin; ommochrome

Figure 1. Model organisms and their contributions to the study of colour changes in the animal kingdom. For each model species, contributions in the fields of evolution, ecology, physiology, cellular and molecular mechanisms of colour changes have been highlighted. A red cross indicates that no study has yet investigated this field for this particular species. A yellow question mark indicates that few studies have started to investigate this field. A green tick indicates that numerous studies have dealt with this field, even though many important biological questions may remain unanswered. (a) The colour‐changing crab spiders Thomisus onustus and Misumena vatia (not shown). Size: few millimetres. Left: Courtesy of Fritz Geller‐Grimm; right: Courtesy of Paul‐Henri Cahier. (b) A desert locust (Schistocerca gregaria) in its solitarious (left) and gregarious (right) phases. Size: few centimetres. Courtesy of Compton Tucker, NASA GSFC. (c) Human‐melanoma derived melanocyte in culture producing melanin (from left to right) and highlighting the process of tanning at the cellular level. Black dots within the melanocyte are melanin‐containing organelles called melanosomes. Cell size: several micrometres. (d) Example of camouflage in a cephalopod, the cuttlefish. Size: several centimetres. Courtesy of Nick Hobgood. (e) Rapid darkening of a rock pool goby (Gobius paganellus) subjected to a dark background (left to right). The same process has been studied in the frog Xenopus laevis (not shown). Size: several centimetres. Reprinted from Stevens M, Lowen AE, Denton AM. 2014 Rockpool gobies change colour for camouflage. PLoS ONE 10, e110325 under the Creative Commons Attribution License. (f) Reddening of a Panther chameleon (Furcifer pardalis) in the presence of a male rival. Size: tens of centimetres. Left: Courtesy of Kris Norvig; right: Courtesy of Eric Mathieu.
Figure 2. Morphological colour changes in a crab spider. (a) At the tissue level, colour‐changing chromatophores of crab spiders are beneath a transparent cuticle and on top of light‐reflecting guanocytes. In white crab spiders, chromatophores possess unpigmented ommochromasomes that do not absorb the incoming light, which is then fully reflected by guanine crystals in guanocytes. During morphological colour change, ommochromasomes progressively mature and acquire yellow ommochromes, such as xanthommatin. Hence, in yellow crab spiders, the incoming light is first partly absorbed by mature ommochromasomes. This transmitted light deprived of blue and violet wavelengths is then reflected by guanine crystals and thus appears yellow to the eye. Courtesy of Fritz Geller‐Grimm. (b) In chromatophores of crab spiders, ommochromasomes can undergo a full cycle of pigmentation and depigmentation, which is the cellular basis of their morphological colour change. (1) During white‐to‐yellow transition, transparent preommochromasomes acquire ommochrome precursors that are slightly yellow. (2) Precursors then form yellow ommochromes leading to a mature ommochromasome. (3) For yellow‐to‐white transition, ommochromasomes enter an autocatalytic process leading to the degradation of their pigments. (4) Degrading ommochromasomes are ultimately recycled into unpigmented organelles, ready for another cycle of ommochrome metabolism. Courtesy of Paul‐Henri Cahier. (c) The production of xanthommatin within maturing ommochromasomes is the molecular basis of their yellow colouration. Thanks to its electronic delocalisation structure, xanthommatin absorbs wavelengths between 400 and 500 nm (i.e. violet and blue). Thus, visible light passing through xanthommatin is deprived of these wavelengths making it yellow (the complementary colour of blue and violet) to the eye. See text for references. Nuc., nucleus.
Figure 3. Environmental and intrinsic factors controlling morphological colour changes. (a) When chromatophores directly sense light stimuli and trigger colour change, it is called a primary response. Colour change can be proportional to the light stimulus, such as in the tanning process of humans. (b) When the visual system is the intermediary between the light stimuli and the chromatophores response, it is called a secondary response. Both neuronal and hormonal systems can be involved in the regulation of colour‐changing chromatophores. Hence, colour‐change pattern can match the light stimuli dynamics. For example, seasonal colour moulting is cyclic because it is linked to the change in photoperiod during the year. One hormonal factor involved in the regulation of skin melanocytes is α‐MSH. (c) From the same pool of premelanosomes, skin melanocytes can produce either black melanosomes containing eumelanins or reddish ones with phaeomelanins. The fate of premelanosomes depends on the balance of two factors, α‐MSH and ASIP; both bind to MC1R at the melanocytic membrane and activate antagonistic signalling cascades. See text for references. ASIP, agouti signalling protein; α‐MSH, α‐melanocyte‐stimulating hormone; MC1R, melanocortin 1 receptor; UV, ultraviolet radiation.
Figure 4. Physiological colour changes at the tissue level in cephalopods. In cephalopods, two layers of chromatophores are involved in colour change: pigmented chromatophores and iridophores. When leucophores are present, they only reflect the incoming light. Cephalopods can produce a wide array of coloured patches using a combination of expanded/retracted pigmented chromatophores together with activated/inactivated iridophores. (a) When pigmented chromatophores are expanded, the incoming light is partly absorbed by pigments and thus appears coloured to the eye (e.g. yellow when absorbed by xanthophores). (b) When iridophores are in an activated state and xanthophores are expanded, a yellow (xanthophores) and a blue iridescent (iridophores) layers are superimposed, leading to an overall green colouration. (c) Another combination is when all pigmented chromatophores are expanded and iridophores are inactivated, the incoming light is then deprived of most of its wavelengths and will thus appear as dark brown.
Figure 5. Factors regulating physiological colour changes at the cellular level. (a) Physiological colour change is mostly a secondary response to light stimuli, although other types of stimuli can be involved, such as temperature (not shown). Both neuronal and hormonal systems can regulate chromatophores responses and thus colour change. (b) Pigmented chromatophores of cephalopods are under the control of a radial neuromuscular system. When radial muscles are relaxed, chromatophores are in a retracted state that do not absorb light. Upon neuronal activity, radial muscles contraction forces chromatophores to expand. As pigmented organelles of chromatophores are tethered together and are located within a cytoelastic saccule, the chromatophores expansion increases light absorption surface. This expanded and coloured state is fully reversible and allows for rapid colour change. (c) Cephalopod iridophores contain iridosomes made of reflectin platelets separated by layers of cytoplasm. In their inactivated ‘off’ state, reflectin platelet structure and layers width do not create light interference and thus colouration. Upon activation of muscarinic receptors by the neurotransmitter acetylcholine, reflectin platelets are phosphorylated, change their conformation and layers of cytoplasm are reduced. The overall effect is the production of light interferences leading to red light. This activated ‘on’ state of iridophores is fully and quickly reversible. (d) In fishes and amphibians, melanophores are the main pigmented cells providing physiological colour change. In their inactivated and unpigmented state, their melanosomes aggregate around the nucleus. Upon binding of α‐MSH to MC1R, melanosomes are moved along microtubules towards their (+)‐end by molecular motors. The dispersion of melanosomes to the edge of the cell increases the surface of light absorption. This activated and pigmented state of melanophores is fully and quickly reversible. See text for references. Ach, acetylcholine; α‐MSH, α‐melanocyte‐stimulating hormone; MC1R, melanocortin 1 receptor; Nuc., nucleus.
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Figon, Florent, and Casas, Jérôme(Aug 2018) Morphological and Physiological Colour Changes in the Animal Kingdom. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028065]