“Evolution is chance caught on the wing.”
—Stuart Kauffman, At Home in the Universe,
paraphrasing a translation of Jacques Monod in Chance and Necessity
AFTER ELEVEN YEARS in the Amazon, having collected 14,712 different animal species (8000 of which were new to science), his body wracked by tropical disease, poor nutrition, and prolonged exposure to sun and heat, and having endured robbery, abandonment by servants, and other deprivations, Henry Walter Bates left the jungle for England in June 1859. His timing was fortunate—in just a few months Darwin’s The Origin of Species would appear.
The two voyagers would fast become great friends. Bates was an immediate adherent to Darwin’s views and he initiated a correspondence that would last more than twenty years, right up until Darwin’s death. Bates was excited and convinced that his observations and collections would lend support to Darwin’s theories. “I think I have got a glimpse into the laboratory where Nature manufactures her new species,” he wrote in one of his first letters to Darwin.
Bates’s greatest contribution was his discovery of what he called “analogical resemblance,” or mimicry. Bates had studied many cases in insects, especially butterflies, where protection was afforded by one species assuming the coloration of another. He noted that birds found certain butterflies to be edible and others noxious. Birds learned to distinguish types based upon only a few experiences. Bates observed that some palatable butterflies mimic the color patterns of unpalatable forms that birds learned to avoid, which affords them protection from predation. This illustration of natural selection in butterflies thrilled Darwin, who told Bates that his paper describing mimicry was “one of the most remarkable and admirable papers I have ever read in my life.” The phenomenon is still known today as Batesian mimicry (figure 8.1).
Darwin continually milked Bates for insights from his vast and superb original knowledge of natural history, particularly for Darwin’s ongoing (and now famous) work on sexual differences and selection. Bates received great encouragement from Darwin, especially to write and publish a narrative of his travels. Not only did Bates draw upon Darwin’s views, but Darwin even reviewed, edited, and wrote an “appreciation” for the one book Bates produced in his entire career, Naturalist on the River Amazons (1863). Darwin had predicted it to be a great success and he was right, for Bates’s writing proved to be superior to either Darwin or his original companion in the Amazon, Alfred Russel Wallace. Bates’s book is still a terrific read today.
Among those 14,000 plus species collected were many butterflies, over 550 species from the region of Ega alone. Bates saw the value of his treasures through a Darwinian lens: “no descriptions can convey an adequate notion of the beauty and diversity in form and colour of this class of insects in the neighborhood of Ega. I paid special attention to them, having found that this tribe was better adapted than almost any other group of animals or plants, to furnish facts in illustration of the modifications which all species undergo in nature under changed local conditions.”
FIG. 8.1 Batesian mimicry. All of the butterflies on the top row are distasteful to birds. Each variation of the swallowtail Papilio dardanus on the bottom row is a mimic of the form above. Note the extensive similarity among each pair of entirely different species. PHOTOS COURTESY OF DR. PAUL BRAKEFIELD, UNIVERSITY OF LEIDEN
Bates continued with my favorite passage: “It may be said, therefore, that on these expanded membranes nature writes, as on a tablet, the story of the modifications of species, so truly do all changes of the organization register themselves thereon.”
He concluded: “Moreover, the same colour-patterns of the wings generally show, with great regularity, the degrees of blood-relationship of the species. As the laws of nature must be the same for all beings, the conclusions furnished by this group of insects must be applicable to the whole organic world; therefore the study of butterflies—creatures selected as the types of airiness and frivolity—instead of being despised, will someday be valued as one of the most important branches of Biological science.”
Bates’s passion for, and convictions about, the value of butterflies to science have been shared by many naturalists, professional and amateur, since he wrote these words 140 years ago. The stories on the expanded membranes of butterfly wings not only delighted Darwin, but William Bateson also paid particular attention in his great book to individuals with atypical patterns. Since then, naturalists have characterized other types of mimicry in butterflies (of other butterfly patterns, of owl eyes, dead leaves, or even bird droppings), and this group of animals has inspired many evolutionary and ecological studies. Of course, the fascination with butterflies extends far beyond conventional scientists. The novelist Vladimir Nabokov had a lifelong passion for butterflies. His expertise supported him, as a curator of Lepidoptera at the Harvard Museum of Comparative Zoology, before his writing achieved wide acclaim.
In this chapter, I will explore the wonderful world of butterfly wing patterns. In this group of insects, the wing has served as a canvas for the evolution of thousands of color patterns. I will focus on the invention of color-patterning systems, and on how so many variations have evolved. We will see that butterflies provide the most exquisite examples of how new patterns evolve when very old genes learn new tricks.
I did not have to travel halfway around the world nor endure any of the hardships Bates did in order to begin to learn about butterflies. My journey began in a parking lot on the Duke University campus in Durham, North Carolina. I was there many years ago to give a seminar on my laboratory’s work, which at the time focused on how genes govern the number and position of bristles on the body of a fruit fly. As is the academic custom when lecturers visit other universities, I was scheduled to meet with a number of Duke’s biology faculty. But one of the professors I was to meet was running late because a pipe had burst in his home. I almost didn’t get the chance to meet Fred Nijhout that day and, had I missed him, not only would this chapter not exist, but I would have missed some of the most thrilling moments I have ever enjoyed in the laboratory.
The bristle patterns of flies has been a great model for understanding some general mysteries in development, such as how structures are located at precise positions on the body. However, in the rush of the few minutes we had crossing that parking lot to get to my next meeting, Fred asked me whether the rules we were finding out for fruit fly bristles could explain his primary love—the patterns on butterfly wings. Frankly, I had no idea.
Whenever I had looked at butterfly wings, accustomed as I was to the pale wings of fruit flies, I just saw chaos. Psychedelic patterns and colors running in all directions. Lines, spots, squiggles, blotches—I couldn’t make out any order (I have the same grasp of modern art). But Fred’s question haunted me for many months. I knew the fantastic lore of butterfly mimicry, predator avoidance, and sexual selection. This was a gold mine, if one could just get some kind of grip on those patterns and the genetic and developmental mechanisms for making them.
Fortunately, Fred soon published a book that served as a primer on all matters of butterfly biology. I learned that one could break down the chaos of those patterns into some order. In the 1920s and 1930s, some comparative biologists perceived an overall plan to butterfly wing patterns. This “ground plan” represented an idealized picture, from which individual species diverged to different degrees. The ground plan consists of several pattern elements near the base of the wing, in the central part, and toward the edge of the wing, which are repeated in each subdivision of the wing that is bounded by veins. These pattern elements consist of sets of bands of different width, as well as the eye-spots (figure 8.2). The subdivisions of the wing are serial homologs, and the patterns within these subdivisions are therefore modular.
FIG. 8.2 The ground plan of possible pattern elements. This schematic represents the idealized spectrum of all possible elements in Nymphalid butterflies. Note the serial repetition of pattern between adjacent wing subdivisions. COURTESY OF DR. H. FREDERIK NIJHOUT, FROM HIS THE DEVELOPMENT AND EVOLUTION OF BUTTERFLY WING PATTERNS; USED BY PERMISSION OF SMITHSONIAN INSTITUTION PRESS
FIG. 8.3 Variation on the ground plan. The three species, Stichophthalma camadeva (A), Fauris menado (B), and Taenaris macrops (C), exhibit different degrees of representation of the ground plan, from virtually all elements to very few. PHOTO COURTESY OF DR. H. FREDERIK NIJHOUT
Butterfly wing patterns are generally composed of some subset of the maximum ground-plan pattern, ranging from species such as Stichophthalma camadeva, which displays most of the ground-plan elements, to those with just a few (figure 8.3). A survey of the thousands of living butterfly wing patterns reveals that diversity is largely a matter of loss of particular elements, or the modification and repositioning of these elements. Patterns that appear more chaotic are due to the dislocation and misalignment of bands between adjacent subdivisions of the wing.
The most crucial observation about these patterns is that each individual band or spot appears to be able to evolve its shape, color, or size independently of other elements. This indicates that the development of individual pattern elements can be uncoupled from one another.
The spectacular beauty and diversity of butterfly wings are due to at least three inventions that took place after this lineage split off from other insects. These inventions include wing scales, coloration, and geometrical patterning systems.
Scales are the fundamental units of butterfly and moth wing patterns. The order to which these bugs belong, Lepidoptera, gets its name from the Greek lepis, meaning scale or flake, and ptera, meaning winged creature. Scales were invented before the elaborate wing-color patterns and probably initially served quite a practical use. If you have ever grabbed a moth in your hand or between your fingers, you have noticed the “dust” residue—these are scales. The easy detachment of these scales is an advantage for these large-winged animals in freeing themselves from sticky places, such as spiderwebs.
Moth and butterfly wings are entirely covered with scales, each of which is the product of a single cell (figure 8.4). Entomologists have believed for a long time that scales evolved as modifications of sensory bristles, becoming flat and wide instead of long and slender, and losing their sensory innervation. This scenario has been borne out by Evo Devo studies. Ron Galant in my laboratory found that developing scales use one of the tool kit genes that is also used for making bristles in the fly, suggesting that scales are indeed modified bristles.
The colors found in butterflies are rivaled by few other insects. Each individual scale is a particular color, which can be seen at high magnification, where individual scales may be an entirely different hue than their neighbors (plate 8a). Any perception of blending or intermediate tones is a visual effect of the spatial arrangement of individual scales of discrete colors. The colors in the wings are due to both chemical pigments and structural colors. Iridescent blues and greens, as well as powdery whites, are the result of the way scales absorb, reflect, and scatter light. Different structural colors are due to very fine differences in scale microanatomy, as well as the combined effects of scale structure and the making of certain chemical pigments.
FIG. 8.4 Butterfly wing scales. STEVE PADDOCK
The geometric patterns on wings are due to the invention and elaboration of developmental pathways that organize them. We know the most about one kind of pattern element, the eyespots. These spots are composed of concentric rings of scales of different colors (plate 8b). Many studies have investigated their role in helping butterflies to evade predators. The proposed role of the eyespots in many species is to deflect the attention of attacking predators (usually birds or lizards) toward the outer edge of the wing, away from the vulnerable main body. Butterflies with even good-size pie slices taken out of their wings can still fly (figure 8.5), whereas a blow to the body can be fatal. The eyespots may draw attention, either because of their conspicuous markings that stand out in contrast to the rest of the wing body or since their resemblance to eyes provokes the predators’ instinct to attack these patterns.
The critical role of eyespots in butterfly defense and their tremendous diversity among species prompted us to concentrate our efforts on understanding how these pattern elements are made and evolve.
FIG. 8.5 Predator damage on a butterfly. This Bicyclus anynana butterfly has been attacked, but because the damage is localized to the edge of the wing, it can still fly and reproduce. PHOTO (TAKEN IN KENYA) COURTESY OF PAUL BRAKEFIELD, UNIVERSITY OF LEIDEN
The adult wing patterns we see are the realization of a process that begins in the caterpillar. Each wing forms from a flat disc of cells that grows enormously during the many stages of larval development (most butterflies have five larval stages). The caterpillar then forms the chrysalis and it is in the chrysalis, just before the butterfly emerges, that the final color pattern is filled in. Though invisible to the naked eye, some parts of the future wing pattern are being made in the caterpillar when the wing is a tiny immature disc, just a fraction of its adult size. This is about a week or more before the adult butterfly will emerge from the chrysalis. In chapter 2, I described one of the most spectacular experiments that revealed early events in butterfly wings, those of Fred Nijhout on transplanting the eyespot focus. Fred showed that the position of the future eyespots is decided in the caterpillar. He discovered that the concentric ring patterns of eyespots are induced by an organizer, the so-called focus, that lies at the center of the developing eyespot.
Because Fred’s transplantation experiments revealed the presence of a novel organizer in the developing butterfly wing, we set about in my laboratory to try to identify genes involved in making the eyespot. Our main questions were: What sort of genetic system generates individual patterns? How did this system evolve? What are some of the genetic tools used to inscribe Bates’s “tablets”? Did the butterflies evolve new genes for making spots, or did they use what was already available?
We had some hunches to go on. My laboratory and several others had made pretty good progress in identifying tool kit proteins involved in making a fruit fly wing. Our logic in tackling the making of butterfly wings was to rely on the evolutionary relationships among insects. Since insect wings evolved just once, then what we knew about the making of fruit fly wings should apply, in general, to the making of butterfly wings. Our hope was, if we were lucky, that studying the butterfly counterparts of the fruit fly tool kit might lead us to clues about the unique features of butterfly wings.
We were lucky.
A team of scientists in my lab isolated from the Buckeye butterfly a number of tool kit genes whose homologs were known to be involved in the building and patterning of fruit fly wings. The presence of these genes in butterflies wasn’t a surprise, nor would that constitute evidence for their role in patterning wings. The key was to see if we could place any of these genes in the scheme of butterfly wing patterning, at the time when transplantation experiments told us that patterns were being set up. To do our experiments, we had to look at where genes were expressed in the tiny wing discs in caterpillars. We wanted to see, through a microscope, hints of how the beautiful patterns that would appear later in the adult were made.
We found that all of the butterfly genes were expressed in parts of the developing butterfly wing disc that corresponded to the same geographical regions where they are deployed in fruit fly wings. This told us that there is a common geography to developing insect wings. The top and bottom surfaces of the butterfly wings, the front and rear of each wing, and the edges of the wing are staked out by the same genes in both species. This is a nice affirmation of the conservation of an ancient wing design. But more intriguing, and exciting, were patterns of gene expression we saw in butterfly wings that had no counterpart in fruit fly wings. I will never forget the moment when my technician Julie Gates called me to the microscope to see the most stunning pattern, of beautiful spots, in the caterpillar wing discs. We saw two pairs of spots on each disc precisely where the eyespots would appear a week later in development, in the positions that Fred Nijhout had defined as the foci of eyespots (plate 8c). Fantastic.
The spots were made by just one of the dozen or so genes we studied. You have already read a lot about this gene—it was Distal-less. This was tremendously exciting because it meant that the same gene involved in building fruit fly limbs and arthropod limbs appeared to be doing something altogether new in butterfly wings. Distal-less still kept its old job: it was also deployed in the distal parts of all developing butterfly limbs, just as in all other insects and arthropods. The spots of Distal-less expression in butterfly wings were a new trick, “learned” long after its ancient role in limb-building (figure 8.6). Remember, everything about a tool kit protein’s action depends on context. Distalless carries out its limb-building role in specific places and times; its job in the wing spots is in another place and time, and controls an altogether different pattern.
FIG. 8.6 A new genetic switch for eyespot expression evolved in the butterfly Distal-less gene. Switches in the Distal-less gene control expression in the embryo, larval legs, and wing in both flies and butterflies, but butterflies have evolved an additional switch to control expression in eyespots. DRAWING BY LEANNE OLDS
How did Distal-less learn the new trick of making spots in the wing? The gene acquired a new switch that responded to the specific longitude and latitude coordinates of these spots of cells. Distal-less spots always form exactly between two veins and along the outer edge of the wing. The precise and reproducible coordinates of these spots tell us that there are tool kit proteins active at these positions that flip on the switch in the Distal-less gene.
The discovery of Distal-less expression in the developing eyespots of the Buckeye butterfly gave us the foothold we were hoping for. It told us that we would be able to make sense out of how these intricate patterns were made. One of the first worries we had to confront was whether we had discovered something general about butterfly wing patterns, or just a peculiarity of this one species. So we looked at how Distal-less was used in other butterflies, both those with and without spots. The correlation was perfect. We saw beautiful spots of Distalless expression in all of the species with spots; we saw no spots of Distal-less in any of the species without spots (plate 8d).
Encouraged by our good fortune, we went looking for other tool kit proteins that might also be expressed in the developing eyespots. We believed that there must be other proteins to discover because eyespots were made of concentric circles of differently pigmented scales; somehow, each ring of scales received different instructions. Fred Nijhout’s experiments suggested that signals from the focus induced surrounding rings of cells to be different colors, depending upon their distance from the focus. Distal-less marked the cells at the center, but the outer rings must also be marked somehow.
We got lucky again. In my lab, postdoctoral fellow Craig Brunetti was searching for other tool kit proteins in butterfly eyespots and he found two more spectacular patterns. When he looked very carefully at the expression of two tool kit proteins called Spalt and Engrailed, he saw that they were expressed in a spot and a ring, respectively, in the African species Bicyclus anynana (plate 8e). The eyespots in this species have a white center, surrounded by a wide black ring, which is surrounded in turn by a gold ring. The Spalt pattern precisely marked the future black ring; the Engrailed pattern did the same for the gold ring. (The detailed correspondence between the rings of protein expression in developing scales and the future rings of the eyespots is exquisite in the color plate.)
Engrailed and Spalt are also very old genes with other jobs, so the explanation for their new role in butterfly eyespot patterning is the same as for Distal-less: the evolution of new switches controlling each gene has enabled these genes to add a new job in butterflies.
Let me briefly interrupt the science here with a little story about the unexpected consequences of unexpected discoveries. It taught me a big lesson about the importance of beauty to general interest in science.
Well after the thrill of first seeing Distal-less in spots, we wrote up our results for formal publication. We quickly found out that not everyone would share our excitement. The journal Nature rejected the paper without further review. Ouch. But, if at first you don’t succeed … So, we sent the article to the journal Science. Its editors were much more receptive and decided to publish our work, and to run a picture of a butterfly wing on the cover of that issue. This was just great for the team—mission accomplished.
However, in other ways, the story was only just beginning.
It usually takes at least a couple of months for a paper to appear, so I had put that article out of my mind when I was later away at a scientific conference. I was staying on a university campus in a dorm room, eating cafeteria food and indulging in the usual glamour of academic science. In between listening to colleagues’ presentations, I received a message to call Nicholas Wade, a science writer for The New York Times.
Baffled, I gave him a ring and discovered that he was preparing a feature story on our article, which was about to appear in Science. I thought this could be neat, something for Mom and my neighbors to read to see how I have used all those years of college and nights in the lab. We had a long discussion and I returned to the meeting and more days of talks.
A little media attention goes a long way. The Times feature prompted many other papers to cover the story. This was summertime, and one prominent newspaper told me they wanted something nice to put on the front page to push the then ongoing, infamous O. J. Simpson murder trial off of page one. So various papers wrote articles about finding “the secret of beauty,” as one story termed it.
Then came TV. I was sitting down to dinner when I recognized a picture of ours being shown on a national news program. Astonished, I kept watching and this was followed by a long video essay by Roger Rosenblatt, who had been prompted by our article to contemplate the question of whether our sense of wonder and beauty is diminished or enhanced by scientific understanding (I think you can guess my opinion).
Months later, Time magazine decided that I should be recognized among a group of young Americans. I wound up in a tuxedo at a dinner with the President, the Washington press corps, and various movie stars and politicians (footnote: a lot of actors are shorter in real life than they appear on screen).
The craziness had one more chapter. Out of the blue, I got a call from a top Hollywood producer who saw the Time article and just wanted to have a chat, in person. Of course, I went to L.A. and we had a great time talking about science, movies, and butterflies.
Okay, so now I get it. Butterflies do inspire broad interest, and I am grateful for that, and my fifteen minutes in the limelight. I still get a lot of good-natured ribbing from colleagues about this whole episode.
Of course, there are critics everywhere, so I can’t resist sharing one piece of anonymous mail I received during my little media circus (figure 8.7). I can’t wait until this guy hears about this book.
In Kipling’s fairy tale, once the leopard got his spots, he was quite contented and would never change again. But butterflies are of a different mind than the leopard, and their evolution has involved changing their spots many, many times. This is obvious when looking at different species, but I will begin with the tale of a butterfly that routinely changes his spots with the changing of the seasons in Malawi.
All I have learned about Bicyclus anynana has been taught to me by Paul Brakefield and his students at the University of Leiden in the Netherlands, and by Vernon French at the University of Edinburgh. Paul has studied this remarkable butterfly for many years in both the field, in Malawi, and in huge populations he maintains in his lab in Leiden.
FIG. 8.7 Fan mail.
In the wilds of Malawi, B. anynana has adapted to the pronounced seasonal differences in its habitat by learning to change its spots. In the wet season, when the foliage is green and abundant, the species bears large conspicuous eyespots on its wings that aid it in surviving attacks from birds and lizards (plate 8f, left). But in the dry season, when the foliage has withered and the leaf litter is brown, and the butterfly must be less active, those large eyespots serve as bull’s-eyes that make the wings stand out against the brown backdrop—screaming, “Here I am, eat me!” So as the weather cools and gets drier at the end of the rainy season, the last broods of caterpillars and chrysalides sense the change, and they emerge instead with no eyespots, just a few tiny little flecks of color where the eyespots would have been (plate 8f, right). These dull brown butterflies will rest hidden on dead leaf litter and wait out the long dry season before the rains return, then they will mate. Their offspring, growing in a warm, humid environment, sense the climate and develop large eyespots that will help protect them in their much more active state.
The adaptation of these butterflies is no “just so” story. Paul and his students have released butterflies with big eyespots in the dry season and found that they are picked off much more frequently than the dull brown, cryptic form, so the evidence for natural selection is clear in the wild. In the laboratory, rearing the developing butterflies at different temperatures reproduces the wild patterns—temperatures of 73° F. (about 23° C.) produce the wet season form; at 62° F. (about 17° C.) the dry season form develops. By shifting the temperature at different stages, Paul’s group determined that the critical period that determined the size of the eyespots was the late caterpillar stage.
When my student David Keys studied Distal-less expression in B. anynana caterpillars raised at different temperatures, he saw an exact correspondence between temperature, the number of cells expressing the Distalless protein, and the size of the adult eyespots. At low temperatures, fewer cells expressed Distal-less in the spots, while at higher temperatures the number of Distal-less expressing cells was much greater. In this species, the eyespot switch in the Distal-less gene responds differently at different temperatures. We do not think that the switch itself senses the temperature directly, but that levels of certain hormones produced elsewhere in the caterpillar’s body vary depending upon the season and temperature. Hormones in insects, just like hormones in our bodies, regulate stages of development and the development of certain tissues. The effects of hormones are ultimately mediated through genetic switches. The Distal-less wing spot switch has evolved a hormone-responsive signature sequence in B. anynana that enables it to respond to environmental changes.
The capacity to control spot development in response to seasonal changes is just one example, albeit a vivid one, of how development and form evolve under natural selection. In the course of butterfly evolution, all sorts of spot patterns have arisen. For example, in the genus Bicyclus alone there are eighty species, which differ from one another in the size, position, and, occasionally, their number of eyespots. This suggests that it is fairly “easy” for butterflies to evolve new wing patterns. There may be a greater degree of freedom in the evolution of possible butterfly wing patterns than in the evolution of other structures. The reason for this flexibility may be that the genetic regulation of wing patterning is organized so that mutations can occur that affect only wing patterns but do not affect other body parts. Evolution in butterflies is very much a matter of “chance caught on the wing.”
We can get a window into the way butterfly wing patterns evolve from the variation in wing patterns seen in the lab and in the wild. Paul Brakefield and his colleagues have isolated a number of very striking, spontaneous mutants with different eyespot patterns. Some of these mutants display no other changes in body pattern. They could represent a class of mutations that, because of the restriction of their effect to the wings, might be viable variations in the wild. Indeed, one of these mutants, named Spotty, displays four eyespots on the forewing instead of the usual two (plate 8g, right). In a closely related species, B. safitza, variants with four eyespots have often been noted in the wild. It is pretty easy then to imagine how the number of eyespots could evolve in this group. Similarly, Paul has isolated mutants that change the color scheme, size, or shape of eyespots (plate 8h) and that thus resemble the sorts of differences that exist among closely related species.
Another angle on the process of wing evolution is the simulation of natural selection by breeding experiments in the lab. In these studies, Paul and his students, instead of birds and lizards, determined the fate of butterflies with spots of different sizes. In any population of butterflies, there are slight variations in the size of the spots. This can be the raw material for natural selection in the wild or “artificial selection” in the lab. Paul and his team established two distinct populations of butterflies, one by selecting and mating butterflies with the largest spots reared at cooler temperatures, and a second line by selecting and mating butterflies with the smallest eyespots reared at warmer temperatures. After about twenty generations of this artificial selection scheme, they obtained populations of butterflies that either made large or small eyespots, independent of temperature (plate 8i).
What happened in these experiments was that the existing variation in eyespot size, which is due to genetic variation in the starting populations of butterflies, was selected for at two extremes (large and small). This resulted in morphologically and genetically different populations. This is, in essence, just what happens in the wild, but over time periods typically much longer than twenty generations.
These explorations into the changeability of eyespots in Bicyclus reveal some of the possibilities in butterfly wing-color pattern evolution, a spectrum that in reality butterflies have done a remarkable job in exploring. Among other eyespot-bearing species, the numbers, sizes, and color schemes of wing eyespots have evolved a fantastic degree of diversity. Underlying the diversity of butterfly wing patterns must be different developmental instructions. The discovery of the Distal-less, Engrailed, and Spalt proteins expression in eyespots has given us ways to see how the many variations on the eyespot theme have evolved in different species.
The most obvious difference between species is the evolution of eye-spot number. The evolution of the number of Distal-less spots in wing discs exactly tracks the evolution of eyespot number. This tells us that evolutionary changes in Distal-less regulation have evolved between species, and it shows how one innovation, the evolution of spots, leads to further diversity in patterns. Once Distal-less-expressing eyespots evolved, tinkering with Distal-less expression produced butterflies with fewer or more eyespots, different-sized spots or, as in B. anynana, seasonal changes in eyespots. These changes in Distal-less regulation were most likely accomplished by changing the signature sequences of the Distal-less gene eyespot switch (figure 8.8).
FIG. 8.8 Modification of the Distal-less eyespot switch explains different eyespot patterns. The evolution of eyespot number (S’ and S”) and the control of eyespot size (S’”) has occurred by changing switches in different ways. DRAWING BY LEANNE OLDS
The changing color patterns of other wing-pattern elements dominate the evolutionary story in most butterflies. The difference in appearance between species, or between individuals of the same species, is due to different spatial patterns of pigment synthesis and scale structural colors. While every species is a story, I will close this chapter by returning to the evolution of mimicry that has played a large role in the discussion of natural selection, and which remains, from the viewpoint of Evo Devo, a mystery yet to be solved.
Striking differences in appearances can often have relatively simple genetic and developmental bases. For example, in the tiger swallowtail (Papilio glaucus) of eastern North America (including Wisconsin!), two forms of the female occur: a yellow form with black tiger stripes, and a black or “melanic” form (plate 8j). This latter type is a specific mimic of the pipevine swallowtail (Battus philenor), which flies in the same range as the tiger but is distasteful to birds. The sharp difference between the yellow and melanic forms of the tiger swallowtail appears to be due to a single genetic difference that determines whether scales in the central region of the wing make a yellow or a black pigment. Even though the pattern differences between individuals appear to be complicated, involving multiple pattern motifs, the genetic differences between forms appear to be relatively few. This also seems to be the case in other examples of mimicry.
The Heliconius butterflies of Central and South America display warning colors, especially reds and yellows, that advertise they are unpalatable. Mimicry occurs among different geographic populations of Heliconius butterflies. Different species in a given geographic region converge on a similar wing pattern, but different geographic populations of these same species may display different patterns. For example, H. melpomene and H. erato appear similar to each other in each locale in Brazil, Ecuador, and Peru, but the different geographic varieties of each species bear different sets of markings (plate 8k). The general idea is that the birds that attack these butterflies differ from region to region and each butterfly species adapts under this selection pressure toward a form that is most effective at discouraging attack by local predators. Extensive genetic studies have been undertaken to attempt to ascertain the genetic differences contributing to the size, shape, and color of bands and rays on Heliconius wings. In general, a modest number of genetic differences appear to control the differences between populations.
Biologists have not yet precisely identified the genes involved in swallowtail or Heliconius color patterns and mimicry. But this is now only a matter of time. When these genes are identified, a great opportunity will arise to make the connections among fitness, genes, and the forms of these marvelous patterns.
While revelations about the mysteries of the evolution of the Technicolor patterns of butterfly wings lie ahead, biologists have recently made some great discoveries about the evolution of one color—basic black—in a host of other animals. The evolution of black or melanic forms is one of the most prevalent color changes in the animal kingdom. In the next chapter, I will tell how the study of black coloration has enabled biologists to capture evolution “in action.”
An African scene, JAMIE CARROLL
