An eyespot (sometimes ocellus) is an

eye An eye is a sensory organ that allows an organism to perceive visual information. It detects light and converts it into electro-chemical impulses in neurons (neurones). It is part of an organism's visual system. In higher organisms, the ey ...

-like marking. They are found in butterflies, reptiles, cats, birds and fish. Eyespots could be explained in at least three different ways. They may be a form of

mimicry In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. In the simples ...

in which a spot on the body of an animal resembles an eye of a different animal, to deceive potential

predator Predation is a biological interaction in which one organism, the predator, kills and eats another organism, its prey. It is one of a family of common List of feeding behaviours, feeding behaviours that includes parasitism and micropredation ...

or prey species. They may be a form of self-mimicry, to draw a predator's attention away from the prey's most vulnerable body parts. Or they may serve to make the prey appear inedible or dangerous. Eyespot markings may play a role in intraspecies communication or courtship; a well-known example is the eyespots on a

peacock Peafowl is a common name for two bird species of the genus '' Pavo'' and one species of the closely related genus '' Afropavo'' within the tribe Pavonini of the family Phasianidae (the pheasants and their allies). Male peafowl are referred t ...

's display feathers. The pattern-forming biological process (

morphogenesis Morphogenesis (from the Greek ''morphê'' shape and ''genesis'' creation, literally "the generation of form") is the biological process that causes a cell, tissue or organism to develop its shape. It is one of three fundamental aspects of deve ...

) of eyespots in a wide variety of animals is controlled by a small number of genes active in embryonic development, including the genes called Engrailed,

Distal-less Genes in the ''DLX'' family encode homeodomain transcription factors related to the ''Drosophila'' distal-less ''(Dll)'' gene. The family has been related to a number of developmental features such as jaws and limbs. The family seems to be well pre ...

Hedgehog A hedgehog is a spiny mammal of the subfamily Erinaceinae, in the eulipotyphlan family Erinaceidae. There are 17 species of hedgehog in five genera found throughout parts of Europe, Asia, and Africa, and in New Zealand by introduction. The ...

Antennapedia ''Antennapedia'' (abbreviated ''Antp'') is a Hox gene first discovered in ''Drosophila'' which controls the formation of legs during development. Loss-of-function mutations in the regulatory region of this gene result in the development of t ...

, and the

Notch signaling pathway The Notch signaling pathway is a highly Conserved sequence, conserved cell signaling system present in most animal, animals. Mammals possess four different Notch proteins, notch receptors, referred to as NOTCH1, NOTCH2, Notch 3, NOTCH3, and NOTC ...

. Artificial eyespots have been shown to reduce predation of cattle by lions.

Zoological distribution

In butterflies and moths

The eye-like markings in some butterflies and moths and certain other insects, as well as birds like the

sunbittern The sunbittern (''Eurypyga helias'') is a bittern-like bird of tropical regions of the Americas, and the sole member of the family Eurypygidae (sometimes spelled Eurypigidae) and genus ''Eurypyga''. It is found in Central and South America, an ...

, serve functions in addition to

mimic In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. In the simples ...

ry; indeed, it is unclear whether they actually mimic eyes. There is evidence that eyespots in butterflies are

antipredator adaptation Anti-predator adaptations are mechanisms developed through evolution that assist Predation, prey organisms in their constant struggle against predators. Throughout the animal kingdom, adaptations have evolved for every stage of this struggle, na ...

s, either in

deimatic display Deimatic behaviour or startle display means any pattern of bluffing behaviour in an animal that lacks strong defences, such as suddenly displaying conspicuous eyespots, to scare off or momentarily distract a predator, thus giving the prey anima ...

s to intimidate predators, or to deflect attacks away from vital body parts. In species such as ''

Hipparchia semele The grayling or rock grayling (''Hipparchia semele'') is a species in the brush-footed butterfly family Nymphalidae. Although found all over Europe, the grayling mostly inhabits coastal areas, with inland populations declining significantly in r ...

'', the conspicuous eyespots are hidden at rest to decrease detectability, and only exposed when they believe potential predators are nearby. Butterfly eyespots can mimic dead leaves for

camouflage Camouflage is the use of any combination of materials, coloration, or illumination for concealment, either by making animals or objects hard to see, or by disguising them as something else. Examples include the leopard's spotted coat, the b ...

from predators, as seen in ''

sexual selection Sexual selection is a mechanism of evolution in which members of one sex mate choice, choose mates of the other sex to mating, mate with (intersexual selection), and compete with members of the same sex for access to members of the opposite sex ...

. Sexual selection drives the diversification of eyespots in different species of butterflies, as mates select for characteristics like size and brightness. Some species of

caterpillar Caterpillars ( ) are the larval stage of members of the order Lepidoptera (the insect order comprising butterflies and moths). As with most common names, the application of the word is arbitrary, since the larvae of sawflies (suborder ...

, such as those of hawkmoths (

Sphingidae The Sphingidae are a family of moths commonly called sphinx moths, also colloquially known as hawk moths, with many of their caterpillars known as hornworms. It includes about 1,450 species. It is best represented in the tropics, but species ar ...

), have eyespots on their anterior abdominal segments. When alarmed, they retract the head and the thoracic segments into the body, leaving the apparently threatening large eyes at the front of the visible part of the body. Butterflies such as the blues (

Lycaenidae Lycaenidae is the second-largest family (biology), family of butterflies (behind Nymphalidae, brush-footed butterflies), with over 6,000 species worldwide, whose members are also called gossamer-winged butterflies. They constitute about 30% of ...

) have filamentous "tails" at the ends of their wings and nearby patterns of markings, which combine to create a "false head". This

automimicry In zoology, automimicry, Browerian mimicry, or intraspecific mimicry, is a form of mimicry in which the same species of animal is imitated. There are two different forms. In one form, first described by Lincoln Brower in 1967, weakly-defended ...

misdirects predators such as birds and jumping spiders (

Salticidae Jumping spiders are a group of spiders that constitute the family (biology), family Salticidae. , this family contained over 600 species description, described genus, genera and over 6,000 described species, making it the largest family of spide ...

). Spectacular examples occur in the

hairstreak The subfamily Theclinae is a group of butterflies, often referred to as hairstreaks, with some species instead known as elfins or by other names. The group is part of the family Lycaenidae, the "gossamer-winged butterflies". There are many tro ...

butterflies; they commonly perch upside down with the false head raised and shift their rear wings repeatedly, causing antenna-like movements of the "tails" on their wings. Studies of rear-wing damage support the hypothesis that this deflects attacks from the insect's head.

In reptiles and mammals

Some reptiles, such as the

sand lizard #REDIRECT Sand lizard {{redirect category shell, {{R from alternative capitalisation{{R from move ...

of Europe, have eyespots; in the sand lizard's case, there is a row of spots along the back, and a row on each side. Many species of

cat The cat (''Felis catus''), also referred to as the domestic cat or house cat, is a small domesticated carnivorous mammal. It is the only domesticated species of the family Felidae. Advances in archaeology and genetics have shown that the ...

, including

Geoffroy's cat Geoffroy's cat (''Leopardus geoffroyi'') is a small wild cat native to the southern and central regions of South America. It is around the size of a domestic cat. It is listed as Least Concern on the IUCN Red List due to it being widespread and a ...

jungle cat The jungle cat (''Felis chaus''), also called reed cat and swamp cat, is a medium-sized cat native from the Eastern Mediterranean region and the Caucasus to parts of Central, South and Southeast Asia. It inhabits foremost wetlands like swamps, ...

pampas cat The Pampas cat (''Leopardus colocola'') is a small wild cat native to South America. It is listed as Near Threatened on the IUCN Red List as habitat conversion and destruction may cause the population to decline in the future. It is named aft ...

s, and

serval The serval (''Leptailurus serval'') is a wild small cat native to Africa. It is widespread in sub-Saharan countries, where it inhabits grasslands, wetlands, moorlands and bamboo thickets. Across its range, it occurs in protected areas, and ...

s, have white markings, whether spots or bars, on the backs of their ears; it is possible that these signal "follow me" to the young of the species. There may be an

evolutionary trade-off In evolutionary biology, an evolutionary tradeoff is a situation in which evolution cannot advance one part of a biological system without distressing another part of it. In this context, ''tradeoffs'' refer to the process through which a trait i ...

in this case between nocturnal camouflage and intraspecific signalling.

In birds

Male birds of some species, such as the

, have conspicuous eyespots in their plumage, used to signal their quality to sexually selecting females. The number of eyespots in a peacock's train predicts his mating success; when a peacock's train is experimentally pruned, females lose interest. Several species of

pygmy owl Pygmy owls are members of the genus ''Glaucidium''. They belong to the typical owl family, Strigidae. The genus consists of 29 species distributed worldwide. These are mostly small owls, and some of the species are called "owlets". The genus in ...

bear false eyes on the back of the head, misleading predators into reacting as though they were the subject of an aggressive stare.

In fish

Some fish have eyespots. The foureye butterflyfish gets its name from a large and conspicuous eyespot on each side of the body near the tail. A black vertical bar on the head runs through the true eye, making it hard to see. This may deceive

s in two ways: into attacking the tail rather than the more vulnerable head, and about the fish's likely direction of travel. The foureye butterflyfish eyespot is thus an example of self-mimicry. For the same reason, many juvenile fish display eyespots that disappear during their adult phase. Some species of fish, like the spotted mandarin fish and spotted ray, maintain their eyespots throughout their adult lives. These eyespots can take a form very similar to those seen in most butterflies, with a focus surrounded by concentric rings of other pigmentation. Deilephila elpenor 11.JPG, Larva of elephant hawkmoth (''Deilephila elpenor'') displaying eyespots when alarmed File:Notodontidae - Cerura vinula.jpg, Larva of puss moth (''Cerura vinula'') in a defensive posture, with black eyespots visible just above its head File:Gray Hairstreak (One more time...) (6222138633).jpg,

Automimicry In zoology, automimicry, Browerian mimicry, or intraspecific mimicry, is a form of mimicry in which the same species of animal is imitated. There are two different forms. In one form, first described by Lincoln Brower in 1967, weakly-defended ...

: gray hairstreak (''Strymon melinus'') has false head at rear File:Zauneidechse 1469 (detail).jpg,

Sand lizard #REDIRECT Sand lizard {{redirect category shell, {{R from alternative capitalisation{{R from move ...

(''Lacerta agilis'') with rows of eyespots File:Glaucidium californicum Verdi Sierra Pines 2 (detail).jpg,

Pygmy owl Pygmy owls are members of the genus ''Glaucidium''. They belong to the typical owl family, Strigidae. The genus consists of 29 species distributed worldwide. These are mostly small owls, and some of the species are called "owlets". The genus in ...

(''Glaucidium californicum'') with eyespots behind head File:Serval from back.jpg,

Serval The serval (''Leptailurus serval'') is a wild small cat native to Africa. It is widespread in sub-Saharan countries, where it inhabits grasslands, wetlands, moorlands and bamboo thickets. Across its range, it occurs in protected areas, and ...

(''Leptailurus serval'') from back, ocelli clearly visible on the ears File:Chaetodon capistratus 14zz.jpg, Foureye butterflyfish (''Chaetodon capistratus'') has false eyes near tail and disruptive eye mask concealing eye

Morphogenesis

Butterfly eyespots are formed during

embryogenesis An embryo ( ) is the initial stage of development for a multicellular organism. In organisms that reproduce sexually, embryonic development is the part of the life cycle that begins just after fertilization of the female egg cell by the male ...

as a result of a

morphogenetic Morphogenesis (from the Greek ''morphê'' shape and ''genesis'' creation, literally "the generation of form") is the biological process that causes a cell, tissue or organism to develop its shape. It is one of three fundamental aspects of develo ...

signalling centre or organizer, called the focus. This induces neighbouring cells to produce specific pigments which pattern the eyespot. Early experiments on eyespot morphogenesis used

cautery Cauterization (or cauterisation, or cautery) is a medical practice or technique of burning a part of a body to remove or close off a part of it. It destroys some tissue in an attempt to mitigate bleeding and damage, remove an undesired growth, or ...

on the butterfly wing eyespot foci to demonstrate that a long range signaling mechanism or morphogen gradient controlled the formation of eyespots in both space and time. The findings cannot be explained by a simple source/

diffusion Diffusion is the net movement of anything (for example, atoms, ions, molecules, energy) generally from a region of higher concentration to a region of lower concentration. Diffusion is driven by a gradient in Gibbs free energy or chemical p ...

model, but could be explained by either a source/threshold model, in which the focus creates the morphogen, or by the sink model, in which the focus generates a gradient by removing a morphogen which was created elsewhere. Several genes involved in eyespot formation have been identified that can fit into these models, but only two of them have been functionally tested. These genes are the

transcription factor In molecular biology, a transcription factor (TF) (or sequence-specific DNA-binding factor) is a protein that controls the rate of transcription (genetics), transcription of genetics, genetic information from DNA to messenger RNA, by binding t ...

Distalless (Dll) and the

ligand In coordination chemistry, a ligand is an ion or molecule with a functional group that binds to a central metal atom to form a coordination complex. The bonding with the metal generally involves formal donation of one or more of the ligand's el ...

(a signalling substance that binds a

cell surface receptor Cell surface receptors (membrane receptors, transmembrane receptors) are receptors that are embedded in the plasma membrane of cells. They act in cell signaling by receiving (binding to) extracellular molecules. They are specialized integra ...

) Hedgehog (Hh). Butterfly eyespot morphology appears to be the result of the

evolution Evolution is the change in the heritable Phenotypic trait, characteristics of biological populations over successive generations. It occurs when evolutionary processes such as natural selection and genetic drift act on genetic variation, re ...

of an altered version of the regulatory circuit which patterns the wings of other insects. This rogue regulatory circuit is able to pattern both the anterior and posterior eyespots independent of the usual anterior/posterior wing compartmentalization restrictions seen in the fruit fly ''

Drosophila ''Drosophila'' (), from Ancient Greek δρόσος (''drósos''), meaning "dew", and φίλος (''phílos''), meaning "loving", is a genus of fly, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or p ...

''. The altered regulatory circuit redeploys early developmental signaling sources, like the canonical

hedgehog A hedgehog is a spiny mammal of the subfamily Erinaceinae, in the eulipotyphlan family Erinaceidae. There are 17 species of hedgehog in five genera found throughout parts of Europe, Asia, and Africa, and in New Zealand by introduction. The ...

(Hh) pathway,

(Dll), and engrailed (En), breaking the anterior/posterior compartmentalization restrictions through increased localized levels of Hh signaling. In turn, this raises expression of its receptor

Patched Patched (Ptc) is a conserved 12-pass transmembrane protein receptor that plays an obligate negative regulatory role in the Hedgehog signaling pathway in insects and vertebrates. Patched is an essential gene in embryogenesis for proper segme ...

(Ptc) and transcription factor. Normally, in ''

'', engrailed acts in the posterior compartment to restrict Ptc and ''

Cubitus interruptus Lambda phage (coliphage λ, scientific name ''Lambdavirus lambda'') is a bacterial virus, or bacteriophage, that infects the bacterial species ''Escherichia coli'' (''E. coli''). It was discovered by Esther Lederberg in 1950. The wild type of ...

'' (Ci) expression to the anterior compartment by repressing transcription of Ci, thereby preventing Ptc expression. From the perspective of

evolutionary developmental biology Evolutionary developmental biology, informally known as evo-devo, is a field of biological research that compares the developmental biology, developmental processes of different organisms to infer how developmental processes evolution, evolved. ...

, understanding the redeployment and

plasticity Plasticity may refer to: Science * Plasticity (physics), in engineering and physics, the propensity of a solid material to undergo permanent deformation under load * Behavioral plasticity, change in an organism's behavior in response to exposur ...

of existing regulatory mechanisms in butterfly eyespot locus development has given more insight into a fundamental mechanism for the evolution of novel structures.

Distal-less

The Distal-less gene is present in almost all eyespot organizers, making it an ideal candidate to carry out major functions of eyespot formation. During the wing imaginal disc development Dll, has two expression domains separated by a temporal component. First Dll is expressed in a group of cells in the center of what will become the focus and eventually the eyespot. This expression starts during the middle of the fifth

instar An instar (, from the Latin '' īnstar'' 'form, likeness') is a developmental stage of arthropods, such as insects, which occurs between each moult (''ecdysis'') until sexual maturity is reached. Arthropods must shed the exoskeleton in order to ...

larva A larva (; : larvae ) is a distinct juvenile form many animals undergo before metamorphosis into their next life stage. Animals with indirect development such as insects, some arachnids, amphibians, or cnidarians typically have a larval phase ...

and lasts until the

pupa A pupa (; : pupae) is the life stage of some insects undergoing transformation between immature and mature stages. Insects that go through a pupal stage are holometabolous: they go through four distinct stages in their life cycle, the stages th ...

l stage. The second domain starts around 20 hours after pupation around the original central cluster of cells, in an area in which a black ring of the eyespot will be formed. Functional experiments using

transgenic A transgene is a gene that has been transferred naturally, or by any of a number of genetic engineering techniques, from one organism to another. The introduction of a transgene, in a process known as transgenesis, has the potential to change the ...

Bicyclus anynana ''Bicyclus anynana'' (squinting bush brown) is a small brown butterfly in the family Nymphalidae, the most globally diverse family of butterflies. It is primarily found in eastern Africa from southern Sudan to Swaziland, Eswatini.Drosophila ''Drosophila'' (), from Ancient Greek δρόσος (''drósos''), meaning "dew", and φίλος (''phílos''), meaning "loving", is a genus of fly, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or p ...

'' fruit flies, Hh is expressed in all cells in the posterior compartment of the developing butterfly wing during the mid fifth instar of butterfly wing development. However, in butterflies, Hh expression is significantly higher in those cells that flank the potential foci. Higher transcription levels of Hh, along with other known associates of the Hh pathway, namely patched (Ptc) the Hh receptor, and cubitus interruptus (Ci), the Hh transcription factor is seen throughout the mid to late fifth instar as well, which further implies a role for Hh signaling in eyespot development and patterning. Furthermore, cells that are flanked by the cells expressing the highest level of Hh signaling are fated to become the foci, indicating that focus cell fate determination relies on high concentrations of Hh in surrounding cells. However, this observation has not been totally confirmed as a rule for multiple butterfly species. Studies tried to extrapolate the result of Hh pathway involvement by looking for the expression of Ci in ''Bicyclus anynana''. Here they observed that both seem to be expressed in eyespots, suggesting a relation with the Hh signaling pathway. However, other studies did not find evidence of Hh expression in ''B. anynana''.

Notch

The Notch (N) gene expression precedes an upregulation of Dll in the cells that will become the center of the focus. This makes N the earliest developmental signal, so far studied, that is related with the establishment of the eyespots. Loss of N completely disrupts Dll expression, and eventually eyespot formation, in several butterfly species. A variety of other wing patterns are determined by N and Dll patterns of expression in early development of the wing imaginal disc, suggesting that a single mechanism patterns multiple coloration structures of the wing.

Evolution

Butterfly eyespots are formed by an interplay of at least 3 genes, namely Distal-less (Dll), spalt (sal), and Antennapedia (Antp), hence their evolution has been shaped by differential expression of these genes in different butterfly taxa, as shown in ''

Bicyclus anynana ''Bicyclus anynana'' (squinting bush brown) is a small brown butterfly in the family Nymphalidae, the most globally diverse family of butterflies. It is primarily found in eastern Africa from southern Sudan to Swaziland, Eswatini. Eyespots painted on the rumps of cows have been shown to reduce cattle predation in Africa. The study authors, Cameron Radford and colleagues, note that in the

Sundarbans Sundarbans (; pronounced ) is a mangrove forest area in the Ganges Delta formed by the confluence of the Ganges, Brahmaputra and Meghna Rivers in the Bay of Bengal. It spans the area from the Hooghly River in India's state of West Bengal ...

, forest users wear face masks with eye markings on the backs of their heads in the hope of reducing tiger attacks. In the study on 2061 cattle in 14 herds over 4 years, 683 were given eye markings, 543 were painted with crosses, and 835 were unpainted. None of the eyed cattle were predated, but 4 cross-marked and 15 unmarked cattle were killed, one by a leopard, the rest by lions. Both the eyespots and the cross markings provided

statistically significant In statistical hypothesis testing, a result has statistical significance when a result at least as "extreme" would be very infrequent if the null hypothesis were true. More precisely, a study's defined significance level, denoted by \alpha, is the ...

protection. The cattle were always in mixed groups of marked and unmarked animals; it is not known whether marking all animals in a herd would provide effective protection.

References

Animal anatomy Antipredator adaptations Mimicry {{DEFAULTSORT:Eyespot (pattern)