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Some butterflies, such as the UK native Peacock butterfly (Google Image Search) have markings on their wings that look just like eyes, complete with a white fleck to imitate a convex, transparency effect, as though the "eye" is reflecting sunlight.

Presumably, this pattern is designed to deter prospective predators, because the predator will see a creature with massive eyes looking at them and think twice before attacking.

But how did the pattern evolve? Was the first one a fluke / a genetic mutation that happened to work, or is there another explanation?

For possible bonus points, is there any way of telling when this occurred, and therefore making a guess as to which creature's eye is being imitated?

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All evolution is due to random changes which are selected for. Change is random, selection is not. –  Ben Brocka Aug 23 '12 at 21:22
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Kahn Academy does an amazing job at this one: Introduction to Evolution and Natural Selection –  Armatus Aug 23 '12 at 22:04
    
@Armatus love Kahn Academy –  LordScree Aug 24 '12 at 11:22
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3 Answers 3

up vote 5 down vote accepted

There has been quite a bit of study on the development of eyespots. How did they evolve is still unclear, but several experiments have elucidated the molecular mechanisms underlying their formation.

The Wikipedia page about eyespots gives a good basic introduction and some interesting references.

So, first of all, how does an eyespot form?

During the development of wings, eyespots arise at specific locations called foci (singular focus).

If you take cells from a focus in a developing wing, and transplant them into another region of the wing, an eyespot will develop at the transplanted site.

Transplanted focus Adapted from: Pattern Formation on Lepidopteran Wings: Determination of an Eyespot - Nijhout, Dev. Biol, 1980

The photo on the left is a normal wing from an adult Buckeye butterfly, Precis coenia. In the middle and right photos, some cells of the big eyespots have been transplanted in a new position during development. As you can see, a third eyespot develops. Note that the middle photo is from an autograph, that is, the cells were transplanted on the same wing. This results in a shrinkage of the normal eyespot. In the right picture, instead, cells were transplanted in another individual, and this does not result in shrinkage of the eyespot.

The authors conclude that:

It is evident from these experiments that the development of the large eyespot on the forewing of Precis coenia depends on the presence of a small group of cells that lie at or near its center. This group of cells corresponds to a "focus": a small region, occurring in each wing cell, that is postulated to be responsible for the induction of most color pattern elements in butterflies and moths (Nijhout, 1978). Cautery experiments establish an upper limit for the size of this focus in the neighborhood of 300 epidermal cells, though it is probable that the actual size of the focus is much smaller.

They further speculate that a specific morphogen may be involved:

The response of the eyespot pattern to cautery or transplantation of the focus is most readily interpreted if we assume that the focus is the source of a morphogen that is somehow able to induce synthesis of specific pigments.

The idea that a morphogen was involved has been confirmed in later years.

From: Development, plasticity and evolution of butterfly eyespot patterns - Brakefield et al., Nature, 1996

The focus is proposed to be a signalling source for a morphogen, the levels of which determine the pigmentation of surrounding cells. Recent investigations have indicated that regulatory genes, such as the Distalless homeobox gene, are specifically espressed in the eyespot focus.

Wing development

During the development of the wing the expression of the Distalless (Dll) protein (shown in green in the picture) corresponds to the location of the future eyespots.

Several mutations exist that will provoke changes in the eyespots patterns. Some of this with the evoking names of Cyclops, Spotty and Bigeye were analysed in the paper.

Now, without going much into insects genetics (which is far from being my domain of interest), you can clearly see that, although the number, position and size of the foci are affected by the mutations, their position always correspond with an increased expression of Dll during development.

wing pattern mutants
Left column: ventral hindwing patterns of a wild type (top), Cyclops (middle) and Bigeye mutants. Right column: forewing pattern in a wild type (top) and Cyclops mutant (bottom).

From the conclusion of the paper (bold mine):

The selection experiments on B. anynana rapidly produced dramatic differences in eyespot size which were due to genes of small phenotypic effect. The mutants described here show that genes also exist with large phenotypic effect on eyespot development (including size) that have no perceptible effect on other wing or body patterns. It is likely that the evolution of eyespot patterns in nature involves both genes with large and small effects on eyespots development. [...]
These observations suggest that the regulation of the eyespot developmental pathway is such that eyespot patterns can evolve rapidly and independently of other wing-pattern elements and body structures.

Finally, another interesting read is:

Wings, Horns, and Butterfly Eyespots: How Do Complex Traits Evolve? - Monteiro and Podlaha - PLoS Biol., 2009

where the authors propose that:

Complex traits require co-ordinated expression of many transcription factors and signaling pathways to guide their development. Creating a developmental program de novo would involve linking many genes one-by-one, requiring each mutation to drift into fixation, or to confer some selective advantage at every intermediate step in order to spread in the population. While this lengthy process is not completely unlikely, it could be circumvented with fewer steps by recruiting a top regulator of an already existing gene network, i.e., by means of gene network co-option. Subsequent modifications of the co-opted network could further optimize its role in the new developmental context.

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Please note: I am not an insect development expert, so I may have missed some important paper/evidence etc. If you know some more that are worth citing please do! –  nico Aug 28 '12 at 0:04
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You're correct with the genetic mutation bit. A basic explanation would be:

Some gene or genes became mutated that lead to the coloration you see, and the end result was that the butterfly or butterflies with the mutated gene were able to produce more offspring or offspring which survived better than the eyeless versions.

There are ways of dating genetic mutations by comparing one organism's genes to another, but accuracy can be an issue without some significant genomic study to confirm mutation rates and other aspects.

However, the butterfly wouldn't be purposefully imitating another creature's eye. It may be by chance and/or predator behaviors that the eyespots look like the eyes of another creature, but the adaptation wasn't a willful act. It was a random genetic mutation or mutations that lead to beneficial coloring, and the eyespots may have improved over time as more mutations occurred.

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Is it possible that the butterfly could have been wilfully imitating another creature's eye, but that the conscious part was genetically mutated out later on? –  LordScree Aug 24 '12 at 11:31
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Possible? I suppose it's possible. However, the likelihood is zero. The chain of mutations and lack of evidence of similar behavior by other butterflies is a Sysiphisian mountain to overcome to prove it happened. The easiest explanation, and the one observed in nature, is that a mutation causes unique coloration. Over time, the butterflies which have the coloration closely resembling eyes are left alone, while those that aren't get eaten - instantly taking them out of the gene pool and leaving only the ones with eyespots. Much, much, much easier. –  MCM Aug 24 '12 at 13:46
    
Good old Occam and his Razor. –  LordScree Aug 24 '12 at 14:39
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I read above ;

''Some gene or genes became mutated that lead to the coloration you see, and the end result was that the butterfly or butterflies with the mutated gene were able to produce more offspring or offspring which survived better than the eyeless versions.''

But, for the genes to mutate randomly, an eye would not form, but a mess. Further, how strange it is, that neither the butteryfly nor the genes are able to see this manifestation. Yet any preditors, from above sees it clearly.

To apply that this random mutation and natural selection, makes up everything that we know, is in itself blind and calls for an eye.

I will state, it is positive variation and nothing more nothing less. No lifeform goes downhill in terms of evolution. Random anything would render any 'random' lifeform , lifeless.

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An eye doesn't need to form with the first mutation. If any marking gives an advantage over non-marked butterflies, that would be sufficient. Then natural selection would refine the mutations to an eye-shape. Evolution acts over multiple generations, always. The butterflies don't have to see what gives them the advantage - as long as an advantage is given, that's enough. I have no idea what you mean by "positive variation," and there's no such thing as "downhill" in terms of evolutionary biology - only better able to survive or less able to survive. Your last sentence is also meaningless. –  MCM Aug 27 '12 at 1:16
    
But, for the genes to mutate randomly, an eye would not form, but a mess: do you have proof of that? An eyespot is a fairly simple round pattern, is not such a complex thing to encode. –  nico Aug 27 '12 at 6:08
    
You just delivered some pretty opinionated statements. What knowledge/science/evidence are you basing them on? Could you please provide references? –  Lubo Antonov Aug 27 '12 at 11:39
    
@MCM - you said 'If any marking gives an advantage over non-marked butterflies, that would be sufficient. Then natural selection would refine the mutations to an eye-shape'. I am sorry, but here you are inferring 'direction' via natural selection. Please, explain how nature performs this selection. The mechanics behind it please? –  user1310 Aug 27 '12 at 13:45
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@user1310: Directionality can occur in evolution, it's just not willfull direction. Say the first mutation creates an amorphous dark blob which survives better than the previous phenotype. Then another mutation occurs where the dark blob gets more circular, and that phenotype survives better than the amorphous. Continue in that vein until you have the current eyespot phenotype. As soon as the eyespot is no longer advantagous, another mutation could enter the population and produce another phenotype. –  MCM Aug 27 '12 at 15:20
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