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Biochemical regulation of pigment motility in vertebrate chromatophores: A

review of physiological color change mechanisms

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DOI: 10.1093/cz/zow051

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 Current Zoology Advance Access published May 20, 2016

Current Zoology, 2016, 0(0), 1–16

doi: 10.1093/cz/zow051
Advance Access Publication Date: 19 April 2016
Article

Article

Biochemical regulation of pigment motility in

vertebrate chromatophores: a review of
physiological color change mechanisms
Russell A. LIGON* and Kristen L. MCCARTNEY
School of Life Sciences, Life Sciences C-wing Rm. 522, Arizona State University, Tempe, AZ 85287-4501, USA
*Address correspondence to R.A. Ligon. E-mail: [email protected].
Received on 25 May 2015; accepted on 21 June 2015

Abstract
The fundamental unit of rapid, physiological color change in vertebrates is the dermal chromato-
phore unit. This unit, comprised of cellular associations between different chromatophore types, is
relatively conserved across the fish, amphibian, and reptilian species capable of physiological color
change and numerous attempts have been made to understand the nature of the four major chro-
matophore types (melanophores, erythrophores, xanthophores, and iridophores) and their bio-
chemical regulation. In this review, we attempt to describe the current state of knowledge regard-
ing what classifies a pigment cell as a dynamic chromatophore, the unique characteristics of each
chromatophore type, and how different hormones, neurotransmitters, or other signals direct pig-
ment reorganization in a variety of vertebrate taxa.

Key words: chromatophore, hormone, neurotransmitter, physiological color change, pigment, vertebrate.

Introduction types of chromatophore associated with physiological color change

in vertebrates, complementing a recently published summary of
In the animal kingdom, there are few phenomena as fascinating as
several of these mechanisms (Sköld et al. 2013). We focus primarily
the ability to quickly change color and pattern, an ability that can be
on proximate mechanisms (i.e., biochemistry and cellular mechan-
used to hide from a predator or communicate with a conspecific.
isms) of rapid pigment translocation, and largely ignore the ultimate
Rapid color change on the scale of seconds to hours, termed physio-
functions (i.e., the selective benefits that physiological color change
logical color change, is typically accomplished via mobilization of
confers) of physiological color change. Why physiological color
pigments or nanostructures within specialized cells called chromato-
phores (Bagnara and Hadley 1973; Aspengren et al. 2009). change has evolved multiple times within vertebrates and how
Although physiological color change has been observed in insects physiological color change confers selective advantages are equally
(Hinton and Jarman 1973), arachnids (Insausti and Casas 2008), interesting topics for discussion, but will not be addressed in detail.
crustaceans (Brown and Sandeen 1948), and cephalopods (Florey Chromatophores are colorful cells that can be classified loosely
1969; Hanlon and Messenger 1988; Messenger 2001), the structures by their overall color but are more accurately designated by their
and mechanisms of invertebrate color change are markedly different color-producing mechanisms or the types of pigments/structures
than those of vertebrates (Umbers et al. 2014). As such, this review that they contain (Aspengren et al. 2009). Pigmentary chromato-
focuses only on color-changing vertebrates (not including the birds phores impart color by selectively absorbing particular wavelengths
and mammals which change color by altering blood flow to exposed of lights, whereas structural chromatophores produce color by re-
skin; Rhodes et al. 1997) so that we might better describe the bio- flecting and scattering particular wavelengths of light with cellular
chemical make-up and regulation of the motile chromatophores re- nanostructures. Among the pigmentary chromatophores that impart
sponsible for physiological color change in these taxa. Specifically, color via absorption of specific wavelengths of light, there are three
the objective of our review is to provide a detailed examination and predominant chromatophore types found in color-changing verte-
description of the signaling molecules that influence the different brates: the black-brown melanophores (which contain melanin), red

C The Author (2016). Published by Oxford University Press.

V 1
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2 Current Zoology, 2016, Vol. 0, No. 0

Figure 1. Schematic representation of the dermal chromatophore unit, shown in the dispersed state.

Notes: The dendritic processes of the basal melanophores, extending around and over the iridophores layer, are filled with melanosomes. Above the iridophores
and the melanophore processes is the xanthophore (or erythrophore layer). Figure reproduced from Bagnara et al. (1968) under a Creative Commons License.

erythrophores, and yellow xanthophores (both of which can contain pigment reorganization (Bagnara et al. 1968; Bagnara and Hadley
either carotenoids, pteridines, or some combination of the two). 1973; Cooper and Greenberg 1992; Grether et al. 2004; Aspengren
Additionally, there are two structural chromatophore types that et al. 2009). In general, the red-yellow erythrophores (or xantho-
imbue organisms with color via reflectance of light: the colorless iri- phores) absorb the shorter wavelengths of light incident upon the
dophores and the white light-reflecting leucophores (both containing dermal chromatophore unit, and the remaining wavelengths are ei-
ther reflected back by the silvery iridophores or absorbed by the
purines; Bagnara and Hadley 1973; Bagnara and Matsumoto 2006;
brown-black melanophores (Bagnara et al. 1968; Bagnara and
Aspengren et al. 2009). All integumentary vertebrate chromato-
Hadley 1973; Nielsen 1978; Aspengren et al. 2009; Figure 2). It is
phore types originate from the embryonic neural crest (Bagnara and
the relative state of pigment dispersion and aggregation in each
Hadley 1973; Fujii 1993; Bagnara and Matsumoto 2006), a migra-
chromatophore, as well as their relative densities, that determines
tory, multipotent cell population (Le Douarin and Kalcheim 1999). how much each contributes to the observed color of skin (Bagnara
As chromatophores mature, they typically form functional associ- et al. 1968; Grether et al. 2004).
ations with each other, termed “dermal chromatophore units”, just It is generally accepted that pigment mobilization must be car-
below the epidermis (Bagnara et al. 1968; Bagnara and Hadley ried out by motor proteins, such as kinesin, dynein, and myosin,
1973). which move along tracks provided by structural elements of the
Considered the fundamental unit of physiological color change cytoskeleton (Bikle et al. 1966; Rodionov et al. 1991; Nilsson and
in vertebrates, the dermal chromatophore unit incorporates melano- Wallin 1997; Tuma and Gelfand 1999; Aspengren et al. 2009). A
phores, erythrophores, xanthophores, and iridophores into an iso- model pathway proposed by Nery and Castrucci in their 1997 re-
lated cellular system (Bagnara et al. 1968; Bagnara and Hadley view describes the general pattern between receptor activation and
1973; Figure 1). This functional unit is capable of producing a wide pigment granule dispersal: First, a rise in intracellular second mes-
range of colors by absorbing or reflecting specific wavelengths of senger (e.g., cyclic adenosine monophosphate ¼ cAMP) concentra-
light (Bagnara and Hadley 1973; Grether et al. 2004). From surface tion is induced by the binding of a signal molecule to its receptor on
of the integument to the base of the dermis, the chromatophore unit the plasma membrane (Nery and Castrucci 1997). Next, the higher
consists of the dendritic processes of the melanophore, a single layer levels of cAMP activate protein kinase-A, which phosphorylates
of xantho- or erythrophores, a layer of iridophores, and the main proteins bound to the pigment granules, causing these proteins to
cell body of the melanophore (Bagnara et al. 1968; Bagnara and detach from the cytoskeleton and allowing the (recently freed) gran-
Hadley 1973; Figure 1). It should be noted that, as conserved as this ule to be transported by kinesin (Figure 3A) away from the peri-
functional unit might be, the relative amounts of each chromato- nuclear area (Nery and Castrucci 1997). Conversely, pigment
phore type and their relative arrangements vary from species to spe- aggregation is typically achieved when protein kinase-A is inacti-
cies and can even vary from one area to another on the same animal vated, leading to protein dephosphorylation, which enables dynein
(Bagnara and Hadley 1973). to transport pigments back toward the center of the cell (Figure 3B).
While the dermal chromatophore unit can be considered to func- This model, while simplified, allows for the generalization that
tion as a single element with respect to color generation, the actual extracellular signals can results in an intracellular cascade that
color reflected is the result of the four individual types of chromato- causes pigment granules to associate with motor proteins to initiate
phores serving different roles by undergoing dynamic, coordinated color change.
Ligon and McCartney  Physiological color change mechanisms 3

Figure 2. Schematic representation of the potential contributions of the different elements of the dermal chromatophore unit to reflected light (i.e., color and
brightness). Light from an external source (e.g., the sun) interacts with the dermal chromatophore, which influences the wavelengths of light transmitted from
the body (and which become visible to external viewers).

Notes: (A) Blue color can be attained when reflecting platelets in the iridophore layer selectively reflect short wavelengths of light and longer wavelengths of light
are absorbed by the melanin-containing melanophore layer. (B) Green or yellowish-green is reflected when the xanthophore layer absorbs short-wavelengths of
light, the platelets in the iridophore layer reflect medium wavelengths of light, and the melanophore absorbs longer wavelengths of light. (C) White light is re-
flected when iridophore platelets reflect or scatter all incoming wavelengths of light. Figure after Bagnara and Hadley (1973).
4 Current Zoology, 2016, Vol. 0, No. 0

Figure 3. Model of melanosome transport during dispersion and aggregation, redrawn from Tuma and Gelfand (1999).

Notes: (A) Long-range melanosome dispersion occurs via transport by kinesin along microtubules. After reaching the cellular periphery, melanosomes are trans-
ported along randomly oriented actin filaments by myosin motor proteins. (B) Melanosome aggregation occurs via microtubules but, in contrast to pigmentary
dispersion, takes place with the aid of dynein molecular motors.

Across vertebrate taxa, the greatest differences in the regulation birds, mammals, and all vertebrates capable of physiological color
of physiological color change depend on whether the integument is change (Aspengren et al. 2009) and this is the only melanin to which
under neural control, endocrine control, or some combination of the we will refer in this review.
two (Nery and Castrucci 1997). However, given the broad range of Melanophores are capable of synthesizing their own melanin
color combinations that can be created by the dermal chromato- (Seiji et al. 1961, 1963) and, based on the final destination of the
phore unit (Grether et al. 2004), an appreciation of the complex melanin produced, can be classified as either epidermal or dermal.
regulatory pathways of each chromatophore type is essential for Epidermal melanophores, responsible for the slower process of
understanding both inter- and intraspecific differences in chromato- morphological color change, are commonly described as “spindle-
phore control. In this review, we examine the effects of hormones, shaped” with varying degrees of dendritic branching and are
neurotransmitters, intracellular second messengers, and even ambi- positioned at the base of the epidermis (Bagnara and Hadley 1973).
ent light on the chromatophores associated with physiological color The cell body of the epidermal melanophore produces melanin gran-
change. ules and the processes, which weave around adjacent epidermal
cells, are the sites of deposition of these granules into other cells
(Bagnara and Hadley 1973). Dermal melanophores, often associated
with the dermal chromatophore unit, are found in the dermis and
Melanophores
consist of a central cell body with dendritic processes that can be dir-
Content and structure ected radially or upward toward the epidermis, giving the cell a bas-
The melanophore’s appearance is affected by the organization of its ket-like shape (Bagnara and Hadley 1973; Nielsen 1978). Dermal
melanosomes (or melanin granules), which are vesicular organelles melanophores retain all synthesized melanin and are, unlike the
that exclusively contain melanin (Bagnara and Hadley 1973). other types of chromatophores, exclusive to vertebrates capable of
“Melanin” is a general term for all members of the tyrosine-derived physiological color change (Bagnara and Hadley 1973).
class of pigments found in melanophores, which have high molecu- Given that color change takes time, even for organisms capable
lar weights and are chemically stable (Lerner and Fitzpatrick 1950; of very rapid color change, there was once a health debate about
Nicolaus and Piattelli 1962; Ito and Wakamatsu 2003). While all whether the dendritic melanophore processes were motile projec-
melanins exhibit these properties, there are several sub-classifica- tions that simply carried melanosomes with them, or if the processes
tions of melanin: neuromelanin, allomelanin, pheomelanin, and were static and only melanosomes translocated within them
eumelanin (Fedorow et al. 2005). Neuromelanin is specifically ex- (Bagnara et al. 1968). However, Bagnara et al. (1968) observed that
pressed in the central nervous systems of primates (Marsden 1961; melanophores in the aggregated state (i.e., melanosomes clustered in
Fedorow et al. 2005), while allomelanin is found in the fungi, plant, the main cell body) possessed membranous layers where once mela-
and bacteria kingdoms (Fedorow et al. 2005). Pheomelanin ranges nophore processes had existed in the dispersed state. This evidence
from a muted yellow to red and is traditionally been recognized only indicated that, in the absence of melanosomes, the processes had
in mammalian and avian melanocytes (Ito and Wakamatsu 2003), simply been emptied and collapsed in place rather than being drawn
though it has also recently been discovered in the shell of Hermann’s back into the cell body of the melanophore (Bagnara et al. 1968).
tortoises Eurotestudo boettgeri (Roulin et al. 2013). Finally, there is Further support for the claim that melanophore processes are per-
the brown-black eumelanin, or “true melanin,” that is produced by manent structures is that the interactions between iridophore and
Ligon and McCartney  Physiological color change mechanisms 5

melanophore plasma membranes are very intimate (Bagnara et al. Regulation of melanosome motility within
1968). For example, even when the melanophore is in the aggre- melanophores
gated state, there are non-random indentations in the iridophore The discovery of motile melanosomes triggered an abundance of in-
plasma membrane corresponding to the locations of known melano- vestigations into the mechanisms and regulation of melanosome
phore processes when dispersed (Bagnara et al. 1968). From this transport within melanophores, especially in species capable of
seminal work, the primary mechanism of physiological color change rapid and possibly facultative color change (see reviews in Bagnara
was determined to be the result of dynamic intracellular pigment and Hadley 1973; Nery and Castrucci 1997; Aspengren et al. 2009;
transportation. Stuart-Fox and Moussalli 2009; Nilsson Sköld et al. 2013). Rapid,
facultative color change has since been studied in a wide variety of
vertebrate species including fish, amphibians, and reptiles (Wright
and Lerner 1960; Bagnara and Hadley 1973; Nielsen 1978; Hadley
Mechanisms of color change
et al. 1985; Okelo 1986; Maeno and Iga 1992; Summers and
Although the specific factors that regulate melanosome motility fre-
Greenberg 1994; Kotz and McNiven 1994; Osorio and Vorobyev,
quently differ among taxa (see below), the mechanics of pigment
1996; Larson and Summers 2001; M€ athger et al. 2003; Logan et al.
translocation within melanophores appear to be relatively conserved
2006). For melanophores, cAMP appears to be one of the most
among different groups. Exactly how are melanin granules trans-
prevalent and consistently agreed-upon cellular regulators of mela-
ported so quickly within the melanophore, especially given their ra-
nosome dispersal (reviewed in Tuma and Gelfand 1999; see also
ther large size (up to several hundred microns in diameter; Bagnara
Fujii 2000). Numerous studies have found that an increase in the
and Hadley 1973)? The process of melanosome translocation is
intracellular concentration of cAMP is associated with a dispersed
thought to be coordinated by the microtubule (MT) and actin fila-
melanosome distribution, whereas a decrease in cAMP causes the
ment architecture of the cytoskeleton and the associated motors
melanophore to reassume the aggregated state (Rozdzial and Haimo
(Bikle et al. 1966; Rodionov et al. 1991, 2003; Nilsson and Wallin
1986; Sammak et al. 1992; Fujii 2000; Logan et al. 2006). In an ex-
1997; Tuma and Gelfand 1999; Figure 3). Specifically, the molecu-
periment by Maeno and Iga (1992), forskolin, a potent activator of
lar motor kinesin transports melanin granules toward the cell per-
the cAMP synthesizing enzyme adenylate cyclase, was administered
iphery during pigment dispersal (Rodionov et al. 1991), where
to melanophores and proved to be a powerful dispersant as well as
melanosomes are subsequently transported along randomly oriented
an effective blocker of induced aggregation. Alpha-melanophore-
actin myofilaments (Tuma and Gelfand 1999; Rodionov et al. 2003;
stimulating hormone (a-MSH) and adrenocorticotropic hormone,
Figure 3A). When melanophores receive input producing melano-
collectively referred to as melanocortins, are also known to activate
some aggregation, the tubulin-based molecular motor dynein hauls
both the cAMP synthesizing enzyme adenylate cyclase and stimulate
melanin granules back toward the nucleus (Nilsson and Wallin
1997; Figure 3B). For example, Logan et al. (2006) showed that melanosome dispersal in reptiles, amphibians, and fish (Hadley and
MTs are essential for melanosome transport in zebrafish Danio rerio Goldman 1969; Goldman and Hadley 1970; Okelo 1986; Maeno
by administering MT disrupting agents and observing that transport and Iga 1992; Fujii 2000).
was diminished, slowed, or eliminated. These authors also investi- Agouti proteins also function in color change processes by antag-
gated the role of actin-based microfilaments and found that they onizing melanocortin receptors and, consequently, counteracting the
may have a role in tethering melanosomes to the periphery of the effects of a-MSH (Cerd a-Reverter et al. 2005; Zhang et al. 2010).
cell after dispersion. This “tethering” could be a mechanism to re- Increased levels of agouti signaling protein are also associated with
duce the cost of color change, by reducing the amount of cellular sig- lighter colors and fewer melanosomes (Guillot et al. 2012). Up-regu-
nalling and energy currency spent to keep the melanophores stellate. lation of specific agouti proteins even appears to underlie the back-
ground matching observed in zebrafish (Zhang et al. 2010),
preventing a-MSH from elevating intracellular levels of cAMP. In
addition to the effects of a-MSH and cAMP on color change, many
Influence on color studies provide evidence that calcium ions (Ca2þ) play an important
In color changing vertebrates, the distribution of melanosomes role in physiological color change via their role as chemical messen-
within dermal melanophores (hereafter “melanophores”), especially gers (Novales and Novales 1965; Van De Veerdonk and Brouwer
in their dendritic processes, is a primary determinant of the lightness 1973; de Graan et al. 1982a, 1982b; Iga and Takabatake 1982).
of the animal’s skin color. That is, as the area of melanosome distri- Despite these empirical results to the contrary, Kotz and McNiven
bution increases, more light is absorbed and a darker color is pro- (1994) assert that there is no evidence indicating a link between
duced. Interestingly, however, melanophore aggregation and Ca2þ concentrations and melanosome motility. Therefore, it seems
dispersal do not appear to be dose-dependent processes in the zebra- that the involvement of calcium ions in the regulation of pigment re-
fish D. rerio. Instead, the melanophores of this species consistently sponses is still somewhat controversial (reviewed in Nery and
demonstrate a translocation threshold where they completely aggre- Castrucci 1997).
gate or completely disperse if at least the minimum dose of trans- While a-MSH is considered a pigment dispersant across all taxa,
location agonist necessary to stimulate pigment migration is two other hormones are associated with pigment cell motility: mela-
administered (Logan et al. 2006). Hence, variation in the extent of tonin and melanin-concentrating hormone (MCH). These hormones
dispersal would refer primarily to the rate of dispersal in this species, can behave as either dispersants or aggregators at different concen-
as the pigment granules move through the intermediate stages of trations in the melanophores of different species (Fujii 2000;
translocation from one extreme to the other (Logan et al. 2006). Aspengren et al. 2009). Melatonin is generally considered an aggre-
The binary nature of pigment dispersion observed in zebrafish may gation inducer in fish, though melatonin sensitivity is highly variable
be species-specific, however, and more work is required to better among species (Nery and Castrucci 1997; Fujii 2000). While it has
understand how broadly this phenomenon extends among color been suggested melatonin indirectly inhibits adenylate cyclase
changing vertebrates. (Filadelfi and Castrucci 1996), supporting its usual role as an
6 Current Zoology, 2016, Vol. 0, No. 0

aggregation agent (Rollag 1988; Sugden 1991; Fujii 1993), mela- has been a great deal of research on the effects of particular com-
tonin can actually elicit pigment dispersion in some fish species (re- pounds, hormones, and neurotransmitters (e.g., a-MSH, MCH,
viewed in Fujii 2000) or even promote opposite responses in melatonin, catecholamines, and cAMP) on the translocation of the
different areas of the same fish’s skin (Nishi and Fujii 1992). melanin granules from the perinuclear area of the melanophore cell
Similarly for MCH, which is typically an aggregator (Oshima et al. body into the dendritic processes. Most of the aforementioned com-
1986; Fujii 2000; Logan et al. 2006; Aspengren et al. 2009), studies pounds act on receptors in the melanophore cell membrane and
have found that high doses of MCH can induce dispersion (within elicit a change in the activity of adenylate cyclase, and therefore a
teleosts). This duality of effect led to the hypothesis that there are change in the intracellular concentration of cAMP. However, several
two different types of MCH receptors with either high or low MCH classes of receptor are frequently present on individual melano-
affinity (Oshima et al. 2001; Aspengren et al. 2009). Reptiles and phores, suggesting that there is a great deal of complexity in the bio-
amphibians are much less sensitive to MCH but, if given in high chemical regulation of melanosome organization and additional
concentrations, MCH can stimulate melanosome dispersal (Wilkes research remains to be done before we can fully clarify the range of
et al. 1984; Fujii 2000). interactions between different receptor types and adenylate cyclase.
Primitive fishes are most susceptible to the influence of the hor- Furthermore, considering the controversy surrounding the role of
mones a-MSH, MCH, and melatonin because, unlike the bony tele- Ca2þ, its relationship to melanophore motility in fish, amphibians,
ost fishes, their physiological color change is mostly controlled by and reptiles should be more specifically investigated. Additionally,
the endocrine system (Fujii 2000). Physiological color change in tele- the melanin pigment is ubiquitous across many more taxa than those
ost fish is also controlled by sympathetic enervation, making them discussed here, and further research has the potential to discover
sensitive to the catecholamine neurotransmitters epinephrine (EPI) and clarify the additional functions it can serve in biological sys-
and norepinephrine (Fujii and Oshima 1986; Maeno and Iga 1992; tems. Moving beyond melanophore-specific examinations, in-depth
Fujii 2000). The sympathetic nervous system is responsible for the investigations of the dynamic interactions between melanophores
flight-or-fight response to stressful stimuli, which is brought about and the other chromatophore types, which produce the remarkable
by the release of catecholamines that can act on either a- or b-adre- color displays of fish, amphibians, and reptiles capable of physio-
noceptors (Maeno and Iga 1992). The roles of a- and b-adrenocep- logical color change, should be a particularly fruitful area of future
tors are conserved across all fish, reptile, and amphibian taxa, and research.
these two types of receptors are often found within the same organ-
ism, either restricted locally or commingling in the plasma mem-
brane of the same melanophore (Vaughan and Greenberg 1987; Erythrophores and Xanthophores
Summers and Greenberg 1994). Stimulation of a-adrenoceptors ini- Content, structure, and color
tiates a decrease in intracellular levels of cAMP concomitant with an Erythrophores and xanthophores are two additional chromatophore
aggregation response, while catecholamines can simultaneously acti- types associated with the dermal chromatophore unit in vertebrates
vate b-adrenoceptors, which induce an increase in cAMP and causes capable of physiological color change. These chromatophores are
melanosome dispersal (Maeno and Iga 1992; Kotz and McNiven loosely classified by their predominant coloration, with xantho-
1994; Nery and Castrucci 1997; Fujii 2000). phores being principally yellow and erythrophores being principally
Competition between a- and b-adrenoceptors was first demon- red (Bagnara and Hadley 1973). For some physiologically color
strated in the green anole Anolis carolinensis by Vaughan and changing vertebrates, including a variety of fish (Satake 1980;
Greenberg in 1987. Because sympathetic nerves do not innervate Hadley et al. 1985; Oshima et al. 1986; Kotz and McNiven 1994;
anole skin, all physiological color change is mediated by circulating Sato et al. 2004) and amphibians (Bagnara et al. 1968; Nielsen
catecholamines binding to adrenoceptors and their respective effects 1978), it has been determined that erythrophores and xanthophores
on adenylate cyclase activity (Vaughan and Greenberg 1987). These are dynamic contributors to color change. However, there is no evi-
authors found that the eyespots of the green anole lack a-adrenocep- dence that this is the case with all color changing vertebrates; there
tors, in contrast to the rest of the anole dermis (Vaughan and may be some species where the erythrophores or xanthophores serve
Greenberg 1987). All other anole melanophores have a- and b-adre- only a passive role, and melano- and iridophores are the only dy-
noceptors, which are both stimulated by EPI (Vaughan and namic chromatophores. For example, there is currently no definitive
Greenberg 1987). The b-receptors of the melanophores are activated evidence of a dynamic contribution of the erythrophore/xantho-
by low levels of EPI and result in skin darkening, whereas high levels phores to the rapid color change of any reptile species.
of EPI stimulate the a-adrenoceptors of those same melanophores to The yellow-to-red coloration of xanthophores and erythrophores
override the b-adrenoceptor response by inhibiting adenylate cyclase is the result of the relative amounts, and types, of pteridine and ca-
and thus the skin lightens (Vaughan and Greenberg 1987). Therefore, rotenoid pigments within each chromatophore (Bagnara and Hadley
an anole under duress will appear green everywhere except for its 1973). Traditionally, there are thought to be only two major pteri-
eyespots, which will be dark brown. Vaughan and Greenberg (1987) dines involved in color change, drosopterin and sepiapterin (Obika
also found that anoles pretreated with a b-specific adrenergic blocker, et al. 1964), though drosopterin can exist in three forms (drosop-
propranolol, prior to treatment with EPI exhibited significantly re- terin, isodrosopterin, and neodrosopterin, all of which are found in
tarded eyespot formation and were unable to attain the maximal the lizard Sceloporus virgatus; Weiss et al. 2012) and xanthopterin
dark brown body coloration. Vaughan and Greenberg (1987) suggest may underlie some orange skin coloration in reptiles and amphib-
that both of these effects occurred as a result of EPI’s ability to acti- ians (Suga and Munesada 1988; Morrison et al. 1995). In compari-
vate only a-adrenoceptors in propranolol-treated animals. son, there are two entire families of carotenoids involved in
physiological color change: the hydrocarbon carotenes and the oxy-
Summary gen-containing xanthophylls (Bagnara and Hadley 1973). However,
The melanophore is an important and dynamic contributor to Chatzifotis et al. (2011) recognize two different classes of caroten-
physiological color change in fish, amphibians, and reptiles. There oids based primarily on the color these molecules reflect: the yellows
Ligon and McCartney  Physiological color change mechanisms 7

(e.g., beta-carotene, lutein, zeaxanthin) and the reds (e.g., astaxan- cytoplasmic periphery, whereas the more numerous carotenoid ves-
thin esters). Because the wavelengths of light absorbed by carotenoid icles of xanthophores are found both near the nucleus and dispersed
molecules (and hence, the wavelengths of light reflected which pro- in the cytoplasm (Ichikawa et al. 1998). While the carotenoid ves-
vide color) are dependent on the length of their conjugated pi-sys- icles were very similar in structure and development in the two chro-
tems (Allen 2008) and not the presence or absence of oxygen, the matophores, there were stark differences in their pterinosome
carotenoid classification suggested by Chatzifotis et al. (2011) repre- ontogeny (Ichikawa et al. 1998). In the xanthophore, development
sents a fundamentally different criterion for grouping carotenoid of the fibrous, concentric whorl (a characteristic property of pterino-
pigments. somes) began at the center of the granule, whereas the whorl de-
The diversity of carotenoid types present in erythrophores and veloped first at the periphery of erythrophore pterinosomes
xanthophores is largely due to the fact that carotenoids can only be (Ichikawa et al. 1998). Also, pterinosomes in the erythrophore re-
obtained through an animal’s diet, as opposed to pteridines which mained uniform in size throughout metamorphosis and on into the
can be synthesized de novo within the chromatophores (Bagnara juvenile frog stages, whereas those of the xanthophore were diverse
and Hadley 1973). Carotenoids are ingested rather indiscriminately, and grew in size during metamorphosis, but then shrunk when the
as different types of carotenoids often coexist within the same food frog completed the transition from tadpole to juvenile (Ichikawa
source, and it is only after ingestion that animals can modify and et al. 1998). It is noteworthy to point out that, in addition to the
metabolically convert the carotenoids according to established bio- pterinosomes of the respective chromatophores being significantly
chemical pathways (reviewed in Møller et al. 2000; McGraw 2006; different in size, these two distinct types of pterinosomes were never
Svensson and Wong 2011). On the other hand, only drosopterin observed to coexist within one chromatophore (Ichikawa et al.
(red) and sepiapterin (yellow) can be produced in abundance de 1998). Given that this study was conducted on a single species, the
novo in the vertebrate taxa examined in this review (Hama 1963; general applicability of these conclusions is not known.
Obika 1963; Bagnara and Hadley 1973; Ichikawa et al. 1998).
While the sepiapterin synthesis pathway has not yet been fully eluci- Mechanisms of color change
dated, it is known that once sepiapterin is formed from guanosine The mechanism of pigment granule reorganization is believed to be
triphosphate, it often serves as a precursor of further pteridine dif- similar, if not the same, in erythrophores and melanophores in
ferentiation (reviewed in Ziegler 2003). However, sepiapterin is not the sense that pigment granules in both cell-types associate with
a precursor to drosopterin; rather there is a branching point in the motor proteins for transport (Byers and Porter 1977; Kotz and
biochemical pathway from which both sepiapterin and drosopterin McNiven 1994; Nery and Castrucci 1997). However, in contrast
are synthesized from the same intermediate (Dorsett et al. 1979). to melanophores, both the aggregation and dispersion processes
Given the shared pathways of pteridine synthesis, it is surprising in erythrophores were approximately twice as fast as melanosome
that individual chromatophores synthesize either drosopterin (eryth- translocation in melanophores (Kotz and McNiven 1994). Further-
rophores) or sepiapterin (xanthophores), to the near exclusion of the more, erythrophore pigments appear to aggregate quickly and with
other type (Ichikawa et al. 1998). uniform velocity, while dispersing with saltatory motions at a slower
Because xanthophores and erythrophores can both contain ca- rate (Byers and Porter 1977; Beckerle and Porter 1983; Kotz and
rotenoid vesicles, pterinosomes, or some combination of the two, McNiven 1994). The difference in dispersal and aggregation behav-
the terms xanthophore and erythrophore are often used interchange- ior of erythrophore pigments is likely due to the structural changes
ably. A commonly used subjective distinction between the two relies in the erythrophore during these different stages (Byers and Porter
simply on whether the chromatophore appears more yellow 1977). Specifically, pigment cells aggregate by moving along
(xanthophore) or red (erythrophore; Bagnara and Hadley 1973). microtubules within a three-dimensional lattice that is also with-
Despite their overall similarity, xanthophores and erythrophores are drawn during aggregation. The restructuring of the collapsed lattice,
distinct entities with subtle, but significant differences. One of these required for pigments to be subsequently translocated away from
differences, exclusivity of pteridine production between chromato- the nucleus (i.e., dispersed), may account for the different rates of
phore types (Ichikawa et al. 1998), has already been discussed. pigment movement between aggregation and dispersal (Byers and
Other differences are related to the development and maturation of Porter 1977). Additionally, the apparent differences in pigment
the chromatophores themselves. In a study of the metamorphosing granule motility between melanophores and erythrophores led Beck-
brown frogs Rana ornativentris, Ichikawa et al. (1998) found that erle and Porter (1983) to investigate the effects of MT disruption
erythrophores were first observed in the hypodermis several stages and actin motility inhibition on pigment motility within erythro-
after the first of the already formed xanthophores were finally mov- phores in squirrelfish Holocentrus adscensionis chromatophores.
ing out of the collagenous layer, where they were formed just above The MT depolymerizing agents colchicine and nocodazole were
the hypodermis, into the subepidermal space that is the residence of used to remove the radial MT cytoskeletal network, beginning at the
mature dermal chromatophores (Ichikawa et al. 1998). As metamor- cell periphery and depolymerizing toward the nucleus (Beckerle and
phosis progressed, the xantho-, irido-, and melanophores assumed Porter 1983). In one treatment, the MTs were partially depolymer-
the arrangement of the typical dermal chromatophore unit, and ized while the pigment granules were retained in a dispersed state by
were eventually joined by the erythrophores, which formed an un- administration of caffeine; after a sufficient amount of depolymer-
usual extra layer below the chromatophore unit (Ichikawa et al. ization had been allowed, EPI was given to induce aggregation
1998). This morphological evidence indicates that erythrophores (Beckerle and Porter 1983). Aggregation only occurred where MTs
and xanthophores originate independently of each other, at least in persisted closer to the nucleus and any pigment left farther out than
R. ornativentris. the MTs extended remained dispersed (Beckerle and Porter 1983).
In R. ornativentris, the major difference between xanthophores In a second experiment, MTs were completely depolymerized with
and erythrophores with regard to the carotenoid vesicles is in their nocodazole, and pigment granules lost their characteristic radial
respective quantities and distributions (Ichikawa et al. 1998). The array and subsequent administration of EPI only induced localized
carotenoid vesicles of erythrophores are generally restricted to the clumping of pigment granules (Beckerle and Porter 1983).
8 Current Zoology, 2016, Vol. 0, No. 0

Therefore, Beckerle and Porter (1983) concluded MTs are required opposed to its bidirectional, dose-dependent influence in fish mela-
for organized pigment translocation. In addition, an actin inhibitor, nophores (reviewed in Fujii 2000). Similarly, MCH also exclusively
cytochalasin B, was administered to erythrophores, but no change to causes aggregation in both erythrophores and xanthophores of sev-
pigment motility was observed, which indicates that pigment disper- eral teleost species (Oshima et al. 1986). While MCH and a-MSH
sion and aggregation in erythrophores is independent of actin, un- are considered antagonizing hormones, MCH can induce aggrega-
like melanophores (Beckerle and Porter 1983). tion in the absence of Ca2þ, unlike the Ca2þ-dependent dispersion
agent, a-MSH (Oshima et al. 1986). Oshima et al. (1986) also tried
Regulation of pigment motility to determine whether the effects of MCH are transduced by a- or b-
In a parallel to melanophore responses to intracellular cAMP levels, adrenoceptors by administering MCH after treatment with either an
calcium ions are the predominant signal for pigment aggregation a- or b-adrenoceptor blocking agent. Although erythrophore pig-
and dispersion in erythrophores (Kotz and McNiven 1994). Kotz ment motility induced by MCH was not found to make use of either
and McNiven (1994) investigated the effect of intracellular calcium adrenoceptor, the neurotransmitters EPI and norepinephrine cer-
ion concentrations (Ca2þ) in the intact, un-lysed erythrophores of tainly do (Oshima et al. 1986). As in melanophores, stimulation of
squirrelfish H. adscensionis and found that an increase in Ca2þ was a-adrenoceptors by catecholamines caused pigment aggregation in
a concomitant, sufficient, and necessary requirement for pigment ag- erythrophores (Oshima et al. 1986). However, despite the coinci-
gregation (Kotz and McNiven 1994). Interestingly, while the rise in dence of a- and b-adrenoceptors on the erythrophores, there was no
Ca2þ is required for aggregation, the pigments remain aggregated mention of catecholamines stimulating b-adrenoceptors and causing
even after Ca2þ has returned to basal levels (Kotz and McNiven pigment dispersal (Oshima et al. 1986). Thus, information regarding
1994). This phenomenon led Kotz and McNiven (1994) to the con- the effects of b-adrenoceptor stimulation of erythrophores in teleosts
clusion that there must be another signaling molecule involved in is lacking. There is also a scarcity of research regarding the effects of
pigment translocation and they turned their attention to the effect of melatonin, MCH, or catecholamines on the erythrophores of rep-
changing cAMP levels on erythrophores, due to the importance of tiles and amphibians; however, this is most likely due to the once
cAMP in melanophore motility. They found that a decrease in Ca2þ prevalent belief that erythrophores only passively contributed to
was necessary for pigment dispersion, but dispersal did not occur physiological color change in these taxa, acting as static filters to re-
unless there was also simultaneous increase in cAMP (Kotz and move particular wavelengths of light (Bagnara and Hadley 1973).
McNiven 1994). While this response is analogous to cAMP’s role in Although light filtering is probably a primary function of erythro-
melanosome dispersion, a high concentration of cAMP in erythro- phores, these chromatophores also appear to provide dynamicity of
phores can apparently be overridden by a sufficient increase in physiological color change in some organisms by varying the extent
Ca2þ. In contrast, melanophore motility was completely unaffected of filtration (Satake 1980; Hadley et al. 1985; Oshima et al. 1986;
by the absence or presence of intracellular Ca2þ (Kotz and McNiven Kotz and McNiven 1994).
1994). The dynamic filtration interaction between ambient light and
Under most conditions, erythrophores (hereafter used to describe erythrophores is perhaps best demonstrated not by chemical induc-
both erythrophores and xanthophores, unless xanthophores were tion, but through pigment motility in response to different wave-
specifically studied) respond to extracellular signals with pigment lengths of available light. In natural conditions, erythrophores are
migration patterns similar to the melanophore responses previously exposed to both the full spectrum of visible light and ultraviolet
described (Oshima et al. 1986; Kotz and McNiven 1994). (UV) radiation; however, the results from a study by Sato et al.
Erythrophores respond to a-MSH administration with pigment dis- (2004) showed that exposure to different wavelengths of light, rang-
persion in teleosts and frogs (Hadley et al. 1985; Oshima et al. ing from 365 (UV) to 600 nm (red end of visible spectrum), affected
1986). In research conducted by Hadley et al. (1985), a super-potent the direction of pigment motility in the Nile tilapia Oreochromis
analog of a-MSH, [Nle4, D-Phe7]-a-MSH or MSH*, was analyzed niloticus. Specifically, Sato et al. (2004) found that erythrophores
alongside a-MSH in the teleost Lebistes reticulatus, five species of dispersed their pigment at 440–550 nm (blue and green light) and
amphibians (genera Rana, Xenopus, Bufo), the lizard A. carolinen- aggregated their pigments at all other wavelengths (365–440 nm,
sis, and a rattlesnake Crotalus atrox. The analog induced prolonged 550–600 nm) as well as in darkness (Sato et al. 2004). These results
darkening in all species and, specifically, dispersion in the teleost make sense because the pigments of erythrophores (and xantho-
erythrophores that lasted 6 days after saline rinse compared with the phores) absorb in the blue and green regions of the spectrum (Allen
relatively fast re-aggregation time of 4 h for melanophores (Hadley 2008). The pigments within erythrophores disperse under these con-
et al. 1985). These results indicate that not only is a-MSH able to ditions because that is when they are capable of maximum absorp-
directly act upon erythrophores in addition to melanophores, there tion, and could provide a protective mechanism to prevent sun
also appears to be significantly different mechanism or potency of damage (Allen 2008).
interaction between the hormone and the two chromatophores
(Hadley et al. 1985). Summary
As in melanophores, the hormones melatonin and MCH also in- Despite reasonably complete knowledge regarding the mechanisms
duce pigment migration in erythrophores (Satake 1980; Oshima of pigment movement within the erythrophores and xanthophores
et al. 1986); however, the catecholamine neurotransmitters EPI and of color-changing vertebrates, much remains to be uncovered. There
norepinephrine have a more direct, one-sided relationship with is a great deal of support for analogous pigment mobilization in the
erythrophores than melanophores (Beckerle and Porter 1983; erythrophores and melanophores of teleosts, yet there has been very
Oshima et al. 1986). Satake (1980) used melatonin as a control ag- little research on the responses of pterinosomes and carotenoid ves-
gregation agent in the xanthophores of the common goldfish icle translocation in the erythrophores of reptiles, amphibians, and
Carassius auratus when testing the effects and interactions of novel other fish species. Given the opposite effects of MCH on fish com-
dispersants; thus, melatonin’s role has so far only been observed to pared with reptile and amphibian melanophores, it is unknown
be an aggregation agonist in the xanthophores of fish species, as whether MCH would aggregate pigments in reptile and amphibian
Ligon and McCartney  Physiological color change mechanisms 9

erythrophores as it does in fish melanophores, or whether MCH The color-producing mechanism within iridophores, guanine, is
would disperse erythrophore pigments as it does in reptile and am- very different from the pigments of melanophores, erythrophores,
phibian melanophores. Additionally, very little research has been and xanthophores in two ways: it is inherently transparent and it is
conducted exploring the effects of melatonin on erythrophores of also a necessary biochemical component of every living cell (Nelson
any of the taxa discussed, and more in-depth investigations concern- and Cox 2008). Unlike melanins, pteridines, and carotenoids, which
ing stimulation of both a- and b-adrenoceptors of erythrophores are serve, for the most part, an accessory role in pigment cells, guanine
certainly needed. is an essential element of DNA and nucleotide-based intracellular
energy currency (Nelson and Cox 2008). In addition, there are other
molecules that occur in iridophores in trace amounts relative to the
Iridophores (with Brief Discussion of abundant guanine, including another essential and ubiquitous pur-
Leucophores) ine, adenine, as well as hypoxanthine and uric acid (Stackhouse
1966; Bagnara and Hadley 1973; Ziegler 2003). Although inher-
Iridophores versus leucophores ently colorless, the tight, but unorganized collection of free guanine
Iridophores and leucophores are frequently lumped together in a sequestered into crystal-like structures imparts a huge refractive
catch-all, “light-reflecting chromatophore” category. Although both index of 1.83 (approximately 75% that of diamond, the most re-
provide color by reflecting light (when compared with pigmentary fractive material known) to the iridophore’s reflecting platelets
colors which imbue color primarily via selective absorption of par- (Land 1972; Fujii et al. 1991; M€ athger et al. 2003; Serway et al.
ticular wavelengths of light), iridophores and leucophores differ 2009). The organization of these highly refractive reflecting platelets
from one another in several key ways. First, leucophores reflect only into stacks throughout the cytoplasm, a medium with a refractive
white light, whereas iridophores can reflect specific spectra of light index of 1.33, results in the iridophore having a very high reflective
ranging from violet to red, including iridescent coloration (Fujii capacity (Land 1972; Fujii et al. 1991). For the iridophores involved
1993; Bagnara and Matsumoto 2006). Second, iridophores tend to in physiological color change, this reflectivity is the result of multi-
be located above melanophores within the dermal chromatophore layer thin-film interference created by the alternating layers of ma-
unit (Bagnara and Hadley 1973), while leucophores are typically terials with high (guanine) and low (cytoplasm) refractive indexes
found below the melanophore layer (Obika 1988). Third, and per- (Denton and Land 1971). In addition to differences in the refractive
haps most importantly, iridophores and leucophores differ with re- indexes between the guanine and cytoplasm layers, the size, shape,
spect to the way that they affect color change. Leucophores are proximity, and orientation of the guanine reflecting platelets influ-
analogous in both form and function to melanophores in that they ence the observed colors. In most biological systems, including all
posses dendritic processes through which motile sub-units vertebrate iridophores studied to date, the reflectivity of multi-layer
(“leucosomes” or “refractosomes”) travel (Fujii and Miyashita thin-film reflectors is “non-ideal” if the optical thickness of all layers
1979; Obika 1988). In contrast, color change is effected within iri- is not uniformly equal (Denton and Land 1971).
dophores by changing the spacing and orientation of orderly distrib-
uted, light-reflecting platelets (Bagnara 1966; Taylor 1969; Fujii
1993; see below). Finally, leucophores are known to contribute to
natural physiological color change in only a handful of vertebrates,
Mechanisms of color change
Another distinctive feature of iridophores is that they have been
located among the ray-finned fishes (killifish Fundulus (Menter et al.
observed to exhibit not one, but two kinds of platelet motion: a slid-
1979); medaka Oryzias (Obika 1988); guppies Poecilia, formerly
ing, lateral dispersion (similar to dispersion in erythrophores) or an
Lebistes (Takeuchi 1976)). However, albino individuals of the
accordion-style stack expansion or compression. Whereas, lateral
African clawed frog also possess leucophore-like cells (Xenopus laevis;
changes in platelet location have been observed only in gobiid fishes
Fukuzawa 2004). Because leucophores are present only in a restricted
(Iga et al. 1990; Fujii et al. 1991), accordion-style changes in stack
subset of color-changing vertebrates, we will focus the remainder of
compression have been observed in the neon tetra (Paracheirodon
our discussion on the factors influencing color changing iridophores.
innesi; Clothier and Lythgoe 1987), blue damselfish Chrysiptera
cyanea (Oshima and Fujii 1987), ornate tree lizard Urosaurus orna-
Content, structure, and mechanisms of color production tus (Morrison et al. 1996), and the panther chameleon Furcifer par-
Iridophores, which contain stacks of colorless guanine platelets, ef- dalis (Teyssier et al. 2015). Regardless of the type of motion utilized
fect physiological color change primarily via the alteration of bright- by iridophores, the end result is a shift in the wavelengths of re-
ness, or relative reflectance, of perceived colors (Bagnara et al. flected light (Fujii et al. 1991; Goda and Fujii 1998). With respect to
1968; Bagnara and Hadley 1973; Cooper and Greenberg 1992). The reflecting platelet movement and concordant color changes, the
organization of the guanine reflecting platelets into stacks causes iri- terms “aggregation” and “dispersion” are not the most precise de-
dophores to provide a highly reflective, often iridescent surface in scriptors of platelet translocation in iridophores (though they are
the dermis of the skin (Bagnara et al. 1968; Cooper and Greenberg sufficient when describing pigment movement within melanophores,
1992; Fujii 1993; Nery and Castrucci 1997). Iridophores do not erythrophores, and leucophores (Fujii 1993; Goda and Fujii 1998)).
contain an actual “pigment” molecule, rather the mutable arrange- The different type of intracellular movement that occurs within iri-
ment of guanine platelets, in conjunction with their high refractive dophores prompted Goda and Fujii (1998) to propose the terms
index, is a dynamic form of structural coloration (Fujii 1993; Prum “LR response” and “SR response,” where LR and SR are abbrevi-
2006). Structural colors are produced by the interaction of light ations for the Longer-wavelength light-Reflecting response and the
with specific, internal or intracellular structures of an organism (Fox Shorter-wavelength light-Reflecting response. Loosely, LR corres-
1976; Prum 2006); interactions that result in perceivable visual ef- ponds to dispersion or increasing the distance between reflecting
fects and colors (from metallic or iridescent to yellow or blue) and platelets (leading to longer-wavelength greens in the blue-green
thus contribute substantially to color changes in the skin (Fujii et al. damselfish Chromis viridis; Oshima et al. 1989), and SR to aggrega-
1991; Cooper and Greenberg 1992; Morrison et al. 1996). tion or contraction of reflecting platelets (leading to shorter-wavelength
10 Current Zoology, 2016, Vol. 0, No. 0

blues in the blue-green damselfish, C. viridis; Oshima et al. 1989) so as In addition to adjusting reflected light on their own, the irido-
to reduce the space between them (Goda and Fujii 1998). phores have a dynamic and synergistic relationship with the erythro-
It is important to note, however, that whether the translocation phores and melanophores of the dermal chromatophore unit
of reflecting platelets is radial or lateral or the iridophores are den- (Bagnara et al. 1968). Bagnara et al. (1968) investigated the inter-
dritic or discoid, all reflecting platelet motility affects the distance actions between the iridophores and melanophores of several frog
between adjacent platelets and, consequently, the wavelength of species and found that when melanophores were in the dispersed
light reflected by the iridophores (M€ athger et al. 2003). According state, the processes of the melanophores, distended with melano-
to M€athger et al. (2003), the reflection of colored light in the para- somes, extend over the top of its associated iridophores thereby pre-
dise whiptail Pentapodus paradiseus depends on both the thickness venting light from reaching the reflecting platelets’ reflective
of the guanine platelets and the distances between them in the plate- surfaces. Conversely, under the influence of melanin aggregating
let stack. Slight changes in the spacing between the platelets can re- agents (e.g., EPI, norepinephrine, MCH), melanosomes are concen-
sult in a significant change in color (Teyssier et al. 2015) since the trated (frequently below the iridophores) and contribute less to cell
highest reflectivity is observed perpendicular to the surface, when color, particularly because the same agents tend to produce long-
the optical thicknesses (actual thickness * refractive index) of the wavelength color shifts among iridophores (Kasukawa et al. 1986,
platelets and spaces are one quarter of the wavelength reflected 1987; Nagaishi and Oshima 1989; Oshima and Kasai 2002) and en-
(Land 1972; M€athger et al. 2003). Fujii et al. (1991) noted in the large their reflecting area, preventing much light from reaching the
dark sleeper (a species of fish Odontobutis obscura) that as reflect- melanin (Bagnara et al. 1968). In other words, the translocation of
ing platelets aggregated (SR response), the skin darkened and re- iridophore reflecting platelets is frequently reciprocal to that of mel-
flected color shifted from longer to short wavelengths (specifically, anosomes and the pigments of erythrophores (but not always;
yellow to blue). Interestingly, Nagaishi et al. (1990) and M€ athger Bagnara and Hadley 1969). Pale coloration in vertebrates that
et al. (2003) also found that the colors reflected by iridophores tran- undergo physiological color change may, therefore, be dependent on
sitioned hue as the angle of incident light changed from the normal the combined effects of iridophore LR response coupled with mela-
(i.e., the colors were iridescent; Doucet and Meadows 2009). This nosome aggregation (Nagaishi and Oshima 1989), whereas skin
phenomenon, predicted by the physical properties of reflecting darkening may primarily the result of melanophore and erythro-
platelets (Huxley 1968; Land 1972) and observed in ex situ skin phore pigment dispersion (Bagnara et al. 1968; Fujii et al. 1991).
preparations (Nagaishi et al. 1990; M€ athger et al. 2003), coupled
with the observed color changes in living fish suggests that motile re- Regulation of reflecting platelet motility within
flecting platelets facilitate a secondary method of color change— iridophores
changing reflecting platelet angle of incidence (Nagaishi et al. 1990). In exploring the factors that regulate iridophore reflecting platelet
According to this “theory of blinds”, named based on the similarity motility, many biochemical regulators have been examined based on
between changes in platelet angle and the movement of the slats of a their well-studied influence on melanophores. For example, one of
Venetian blind, shifts in spectral peaks (i.e., hue and brightness) can the first investigations into the hormonal factors influencing platelet
also arise due to changes in the orientation of reflecting platelets movement in amphibians discovered that reflecting platelets aggre-
within the iridophore layer (Nagaishi et al. 1990). In an impressive gated in response to the potent melanophore stimulating agent a-
study, the Venetian blind model has recently been convincingly and MSH, but were otherwise dispersed to provide the maximum sur-
empirically validated as a potentially significant force contributing face area for reflectance (Bagnara et al. 1968). The relationship be-
to the rapid color change exhibited by organisms with motile irido- tween a-MSH and reflecting platelet aggregation also appears in
phores (Yoshioka et al. 2011). several fish species (dark sleeper O. obscura, Iga et al. 1990; Fujii
et al. 1991; blue-green damselfish C. viridis, Oshima et al. 1989).
Relationships with other chromatophores However, this relationship is not universal, as the reflecting platelets
Since Bagnara et al. (1968) proposed the structure of the dermal of ornate tree lizard U. ornatus iridophores do not respond to ex-
chromatophore unit, there has been little deviation from this arch- ogenous administration of MSH (Morrison et al. 1996), nor do
type across diverse taxa of vertebrates capable of physiological color those of blue damselfish (C. cyanea, Kasukawa et al. 1987) or com-
change. The iridophores associated with color change are seques- mon surgeonfish (Paracanthurus hepatus, Goda and Fujii 1998).
tered beneath a layer of erythrophores and within the upward-ex- Additionally, research by Iga et al. (1991) showed that a-MSH-
tending dendritic processes of melanophores (Bagnara et al. 1968). induced aggregation was inhibited in the absence of Ca2þ, indicating
Although iridophores are usually part of the dermal chromatophore that platelet motility may depend, as with pterinosomes and carot-
unit, there is no general model which can capture the ratio of irido- enoid vesicles, on intracellular Ca2þ concentrations. Maeno and Iga
phores to melanophores (or erythrophores) because the number of (1992), who found that MSH caused dispersion in melanophores by
iridophores associated with an erythrophore or encased by a mela- activating adenylate cyclase and thereby increased intracellular
nophore is highly variable (across taxa, within species, and among amounts of cAMP, presented evidence that the iridophores of the
different regions of the same individual; Bagnara et al. 1968). dark sleeper O. obscura also respond to increasing concentrations of
Although there are many ways in which iridophores differ from mel- cAMP by aggregating reflecting platelets. Administration of the
anophores and erythrophores, one peculiar difference is that there is potent adenylate cyclase activator forskolin or a cAMP analogue
no single description of an iridophore that is representative of them (8-bromoadenosine 30 ,50 -cyclic monophosphate, or 8-Br-cAMP) re-
all (Iga et al. 1990; Fujii et al. 1991; Teyssier et al. 2015). That is to sulted in the SR (platelet aggregation) response of reflecting plate-
say, no one model of an iridophore can capture both the radial and lets, but whether a decrease in cAMP levels was sufficient for
lateral types of reflecting platelet motion, nor account for the obser- dispersion was not examined (Maeno and Iga 1992). However, Fujii
vations of iridophores being either non-dendritic, like erythro- et al. (2000) postulated that the overall result of a-MSH is aggrega-
phores, or dendritic, in which the reflecting platelets disperse into tion in teleostean iridophores and that a-MSH does so by inhibiting
the processes as in melanophores (Iga et al. 1990; Fujii et al. 1991). adenylate cyclase activity. This claim, when compared with the
Ligon and McCartney  Physiological color change mechanisms 11

findings of no effect for MSH on ornate tree lizards, blue damselfish, MCH, MSH, and melatonin upon the iridophores of different spe-
or common surgeonfish, makes generalizations regarding the effects cies, it is very likely that the chromatophores of different species or
of a-MSH or changes in cAMP concentrations on translocation of taxa respond differently to various hormones because of inherent
iridophore reflecting platelets impossible across all taxa. variation in hormone receptor types, locations, and abundances.
Inconsistent findings regarding the effects of certain hormones or In stark contrast to the conflicting results concerning a-MSH,
chemicals on reflecting platelet movement within iridophores are MCH, and melatonin, there is consistent agreement regarding the ef-
not restricted to investigations of a-MSH. There is just as little con- fects of catecholamine neurotransmitters upon fish iridophores. In
sistency in the investigations of melatonin and MCH in fish irido- multiple studies, norepinephrine was found to elicit the dispersive,
phores. Iga et al. (1990) and Oshima et al. (1989) observed the LR LR response in the iridophores of teleosts by binding to a-adreno-
(dispersed) response of iridophores after treatment with melatonin ceptors (Fujii 2000), specifically in the following species: the dark
in the gobiid dark sleeper O. obscura and blue-green damselfish C. sleeper (O. obscura, Fujii et al. 1991), the freshwater goby (O.
viridis, respectively. Similarly, Oshima et al. (1989) also observed obscura, Maeno and Iga 1992), and the common surgeonfish (P.
the dispersal of reflecting platelets in response to MCH in C. viridis. hepatus, Goda and Fujii 1998). Furthermore, Maeno and Iga (1992)
However, MCH had no influence on iridophore motility in the blue determined that the freshwater goby iridophores only possess a-
damselfish C. cyanea (Oshima et al. 1986), and neither melatonin adrenoceptors and that a-adrenoceptor blockers effectively inhibited
nor MCH had any effect on reflecting platelet motility of the com- norepinephrine-induced dispersion (Goda and Fujii 1998).
mon surgeonfish P. hepatus (Goda and Fujii 1998). This inconsist- As with melanophores and erythrophores, iridophores of several
ency, just within teleost fish, illustrates that the effects of MCH, species also appear to dynamically respond to local environmental
melatonin, and even MSH on iridophore reflecting platelet arrange- conditions. For example, the reflecting platelets of neon tetra P.
ment are currently indeterminate. Considering the variable effects of innesi respond to light by exhibiting the LR response (Lythgoe and

Figure 4. Photographs of an individual male eastern fence lizard Sceloporus undulates exhibiting (A) blue coloration at warm temperature (28.8 C) and (B) green
coloration at cool temperature (24.6 C).

Note: Photographs courtesy of Tracy Langkilde.

12 Current Zoology, 2016, Vol. 0, No. 0

Shand 1982). Specifically, Lythgoe and Shand (1982) found that and temperature, chromatophores undergo rapid pigment reorgan-
shining a white light on the lateral stripes of tetras caused an in- ization to produce a wide array of chromatic changes. Depending on
crease in the distance between adjacent reflecting platelets and an the stimulus, different chromatophore types respond with either dis-
associated shift toward reflecting more long-wavelength light, even persion to maximize their relative contribution to the overall color
in decapitated fish. Subsequent investigation of neon tetra irido- produced, or aggregation to minimize their effect. Here, we have at-
phores uncovered the presence of an opsin-based visual pigment tempted to review the similarities and differences between melano-
located within the iridophores, suggesting a mechanism for the pho- phores, erythrophores, xanthophores, and iridophores, as well as
toresponsiveness observed in these chromatophores (Lythgoe et al. how these different classes of chromatophores can rapidly confer
1984). In addition to light, the reflecting platelets in ornate tree liz- specific colors to the dermis through a coordinated effort.
ard iridophores have been shown to respond to localized changes in One important conclusion concerns the reciprocal relationship
temperature (Morrison et al. 1996). Specifically, heating the ventral, between iridophores and the other types of chromatophore.
belly of skin of these lizards caused a reduction in the predominant Iridophores, located within the basket-like projections of the mela-
wavelength of reflected light, causing an observed change in color nophore, appear to frequently be dispersed to their maximum re-
from coppery/green to an intense blue (Morrison et al. 1996). flecting surface area when the overlying erythrophores are punctate
Similar, temperature-dependent changes in structural coloration and the melanophore processes are devoid of melanosomes. This re-
have been observed in the eastern fence lizard (Sceloporus undula- lationship diminishes the colorful contribution of the melanophores
tus, Langkilde and Boronow 2012; Figure 4). Although the specific and erythrophores and enhances the reflective capacity of the irido-
mechanisms by which increases in temperature alter reflecting plate- phores; this is the light or pale state. In the dark state, iridophores
let spacing in these lizards are currently unknown, it has been postu- are aggregated and obscured by both the dispersed melanophores
lated that these color changes serve as a signal of thermally and erythrophores; therefore, color absorption is maximized and re-
dependent performance capability which could be used during intra- flectivity diminished. The likelihood of a general, oppositional re-
sexual contests (Langkilde and Boronow 2012). sponse for iridophores, coupled with the sparse literature regarding
reptilian and amphibian iridophores, suggests that investigations of
Summary the iridophores of all the classes of vertebrates (and their intracellu-
Evidently, there has been a plethora of research investigating the lar transduction pathways) would greatly benefit the study of chro-
biochemical regulators of reflecting platelet translocation in fish iri- matophores and color change. There is also room for future inquiry
dophores, but relatively few investigations of reflecting platelet mo- into the physiological regulation of the erythrophores of reptile and
tility in amphibians or reptiles (with a notable recent exception; amphibian species, as there is a similar lack of research of their
Teyssier et al. 2015). Additionally, the specific mechanisms of re- physiological regulation compared with the abundance of informa-
flecting platelet translocation are well-understood in just a few spe- tion regarding fish erythrophores.
cies of fish. As in the previous discussions of erythrophores and Although our primary focus in this article was to review the cur-
melanophores, broad generalizations across taxa cannot be made rent understanding of the cellular and biochemical processes under-
with respect to hormones, neurotransmitters, or other chemicals af- lying physiological color change, examining color change in an
fecting reflecting platelet translocation. Even the abundant evidence evolutionary context may yield new and exciting insights.
describing fish iridophores is somewhat inconsistent and controver- Understanding how the ability to rapidly change color evolved, as
sial at larger taxonomic levels, such that generalizations should be well as how social and environmental factors might influence the
limited even within fish. An important exception to this rule is the evolution of color change (e.g., Stuart-Fox et al. 2007; Stuart-Fox
effect of optical thickness on reflected wavelength (Land 1972; and Moussalli 2008), could offer key insights into certain mechan-
M€athger et al. 2003) because this relationship addresses physical isms of chromatophore activity and function. Although we focused
properties of materials, which are constant despite the organism or on chromatophore responses to particular neural or hormonal sig-
cell in which they are found. Although there is potential for further nals and excluded discussions of how or why chromatophores are
research in many directions, there are three areas that would most stimulated, determining the reasons for organisms to undergo
clearly benefit from future study. The first would be determining the physiological color change is a crucial next step toward understand-
mechanism for platelet transport, especially given that there are two ing the entire process of chromatophore control and function.
different kinds of motion, radial and lateral, which have been Stuart-Fox and Moussalli (2009) put forth an intriguing review
observed in various iridophores. Next, a more in-depth and consist- of three of the most prominent functions of physiological color
ent understanding of the effects of aggregation and dispersion agon- change: camouflage, communication, and thermoregulation. While
ists such as a-MSH, MCH, and melatonin as well as the roles of color change is often used for background matching (Zoond and
cAMP and Ca2þ as second messengers would allow clearer discourse Eyre 1934; Okelo 1986; Vroonen et al. 2012; Stevens et al. 2014),
when comparing iridophores to other chromatophore types or when animals with dynamic color change abilities could potentially em-
discussing the dermal chromatophore unit as a whole. Finally, much ploy multiple camouflage strategies in response to different predator
as with the erythrophore, there is a relative dearth of comparative types (Stuart-fox et al. 2008; Stuart-Fox and Moussalli 2009). Such
information regarding iridophore motility in reptile and amphibian facultative, predator-specific crypsis was described by Stuart-Fox
species capable of physiological color change. and Moussalli (2008) in Smith’s dwarf chameleons Bradypodion
taeniabronchum. Using model predators, these authors found that
chameleons responded with better background matching for avian
Conclusions predators than for snakes, taking into account the different visual
Physiological color change is the result of dynamic pigment move- systems of the predators. Whereas the objective of camouflage is to
ment of multiple chromatophores and their interactions with each avoid detection or recognition by predators or prey (Stevens and
other within the dermal chromatophore unit. Regulated by hor- Merilaita 2009), social selection frequently favors conspicuous col-
mones, neurotransmitters, and even environmental cues such as light oration and rapidly changing color signals for use in intraspecific
Ligon and McCartney  Physiological color change mechanisms 13

communication (Stuart-Fox and Moussalli 2009). Animals capable related to physiological color change. The questions that remain to
of physiological color change have the benefit of communicating be answered involve fully understanding the mechanisms behind
with transient, conspicuous color signals, but may experience pigment organelle locomotion; the evolutionary pathways of color
reduced predation risk relative to species that display long-term, change; determining the importance of and interactions between the
static coloration or patterns (Stuart-Fox and Moussalli 2009). various functions of color change; and whether there are previously
Therefore, rapid color change can facilitate courtship or be used to unknown or unexamined receptors, stimuli, or biochemical path-
signal during aggressive interactions (e.g., Summers and Greenberg ways that affect chromatophores and physiological color change.
1994; O’Connor et al. 1999; Höglund et al. 2002; Ligon and
McGraw 2013; Ligon 2014) without sacrificing the ability to remain
inconspicuous after these brief intraspecific encounters (Stuart-Fox Acknowledgments
and Moussalli 2009). The authors thank K.J. McGraw, M.W. Butler, and two anonymous re-
Color change can also serve in a homeostatic capacity by helping viewers for providing helpful comments on previous versions of this article.
to regulate body temperature (Norris 1967) and, for amphibians, R.A.L. was supported by the ASU Graduate College Completion Fellowship
possibly water balance (Stegen et al. 2004; Stuart-Fox and Moussalli and National Science Foundation Grant no. 1401236 during the creation of
this article.
2009). The vertebrates that undergo true physiological color change
(i.e., through pigment translocation rather than increased or
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