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Pattern Formation Explained by Evolution? Not So Fast

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Few are the scientific papers that try to explain animal patterns: zebra stripes, butterfly colors, the beautiful designs on tropical fish. The mathematical precision of plant spirals, called phyllotaxis, shouts for explanation. Unquestionably, genes are involved, but where did the genes come from? Why do they turn on and off in specific ways to produce patterns? How are these to be explained by unguided material processes? A few recent papers try to answer these questions, sometimes erring on the side of overconfidence.

Chipmunks

“Understanding the origins of variegated colour patterns in mammalian fur is an abiding problem in biology,” Nature says in an editorial. “Other animals adopt a range of pigments, and even use optical effects such as iridescence to lend a chromatic gloss, yet the mammalian palette is mainly monochrome. A patch of skin either contains melanocytes, or it doesn’t.” Moreover, “The pattern starts to emerge long before a mouse is born.” Something deep within the neural crest is taking place during development. Differences in pigmentation patterns are often implicated with other phenotypic traits. “The script runs deep, with many layers of meaning.”

How does a monochrome process yield spots on a jaguar, and the stripes on a mouse or chipmunk? The editors take some comfort in a study published in the same issue of Nature that identified differences in gene expression in the light and dark stripes of the African striped mouse. Here’s what Mallarino et al. found:

Mammalian colour patterns are among the most recognizable characteristics found in nature and can have a profound impact on fitness. However, little is known about the mechanisms underlying the formation and subsequent evolution of these patterns. Here we show that, in the African striped mouse (Rhabdomys pumilio), periodic dorsal stripes result from underlying differences in melanocyte maturation, which give rise to spatial variation in hair colour. We identify the transcription factor ALX3 as a regulator of this process. In embryonic dorsal skin, patterned expression of Alx3 precedes pigment stripes and acts to directly repress Mitf, a master regulator of melanocyte differentiation, thereby giving rise to light-coloured hair. Moreover, Alx3 is upregulated in the light stripes of chipmunks, which have independently evolved a similar dorsal pattern. Our results show a previously undescribed mechanism for modulating spatial variation in hair colour and provide insights into how phenotypic novelty evolves. [Emphasis added.]

The editors think it odd that the mouse and the chipmunk ended up with very similar patterns. “Chipmunks are more closely related to squirrels than to mice: the last common ancestor of mouse and chipmunk lived when dinosaurs did,” they say. “Yet the formation of chipmunk stripes is governed by essentially the same processes that create the patterning in mouse skin, even though the mechanisms might have evolved independently in each case.” Sure enough, Mallarino et al. appeal to “convergent evolution” to explain it. Giving something a name, however, is not the same as understanding it.

Phys.org‘s summary of the paper pretends the matter is now understood, offering a Kipling-like story, “How the African striped mouse got its stripes.” BBC News implies the chipmunk “earned its stripes.” But identifying a gene that’s involved, and giving it a name Alx3, does little to explain why a chunk of DNA in the dark of a cell’s nucleus produces parallel stripes along the rodents’ backs. And surmising that “these stripes may play an important role in helping the mice escape predators” does little to link a physical cause to an effect. If this were a law of nature, every prey animal would have stripes — but lab mice do not. An astute critic, furthermore, might well ask why the predators didn’t evolve the ability to see through this trick since the time of the dinosaurs. Phys.org starts with chutzpah but ends with humility, admitting that the process is not understood.

Looking forward, the researchers would like to understand what controls where Alx3 is expressed, and whether variation in the timing and location of Alx3 expression can explain the evolution of novel color patterns in nature. “The next step is to figure out what controls Alx3 expression,” said Mallarino. “Can you just tinker with where and when Alx3 is expressed to generate a diversity of striping patterns? We don’t know the answer, but that is something we are excited about,” added Hoekstra.

In the BBC article, Hopi Hoekstra, the well-known Harvard evolutionary biologist, admits that “Overall, we know very little about how pigment patterns form, especially in mammals.”

Butterflies

Researchers from three countries, America, England, and Germany, think they have figured out how one genus of butterfly makes its iridescent blue color. Publishing in Nature‘s open-access journal Scientific Reports, they found a simpler optical trick is involved than previously thought. The “Blue Diadem” butterfly from Africa doesn’t need to rely on a “complex ridge-lamellar architectures in the upper lamina of the cover scales.” Instead, “the lower thin lamina in the white cover scales causes the blue iridescence.” Optical interference, similar to the colors produced by a thin film of oil, produces the intense blue seen on the butterfly’s wings. If you crush the wing with your fingers, you won’t see any blue. You’ll have brown dust from the disrupted layers of brown and white layers of scales. They only looked blue when stacked very precisely in “photonic crystals” that cause optical interference.

That’s a start, for sure, but it only begins to explain the overall effect. The butterfly pictured in the paper looks like a work of art. What process placed the cover scales into the exact positions that yield a complex, symmetrical pattern of blues, whites and blacks that humans find beautiful? How did this happen inside a chrysalis automatically via genes over which the developing insect exercises no conscious control? The authors seem to realize there are wonders here beyond their comprehension:

Many butterflies (Order: Lepidoptera) possess very fascinating colouration, and most species of butterfly can be identified solely by the colour pattern on their wings. Such a diversity has attracted a wealth of research to determine the mechanisms responsible for such colours. From a functional perspective, wing colouration can be important in a multitude of ways, ranging from mating, camouflage and warning purposes. Moreover, structurally unique, visually chromatic and complex colour mechanisms found in numerous butterfly wings inspired various advanced technical applications. For example, a hierarchical multilayer air-cuticle pattern inspired by Morpho butterflies was mimicked for selective gas sensing and colourful hydrophobic coatings. Colour mixing due to multilayer microcavities inspired from Papilio blumei was replicated for polarization-sensitive optical signatures. The reverse diffracting grating effect of Pierella luna was copied artificially and might be useful for bio-sensing and anti-counterfeiting. Hence, analysing butterfly colour patterns does not only enrich our understanding of inter/intra-specific communication and the evolution of exaggerated signalling of butterflies, it can also be the source of new photonic devices.

They point out another wonder of nature that defies evolution. A completely unrelated species uses the same optical trick. “A similar colouration mechanism is also found in the feathers of the bird Steller’s Jay where the colour difference of white and blue feathers arises primarily due to the inherent melanin pigment content difference below spongy nanostructures.” Once again, the optical principle is only part of the story. Understanding how and why genes build these structures in particular patterns would require additional explanation.

Plants

We’ve discussed previously the wonder of phyllotaxis. This is the observation that many plants, including sunflowers, cacti, and artichokes, produce spiral patterns that follow the Golden Ratio and the Fibonacci Series. Whenever scientists offer an explanation we get excited, thinking that an unguided mechanism has finally been discovered that can explain it. This month, Current Biology steps up to the plate with an open-access paper by Batia et al., entitled, “Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.” Readers can opt for the quick summary in Phys.org, “Feedback loop behind spiral patterns in plants uncovered?” The question mark suggests some doubt about the explanation.

How do plants create such amazing patterns? Based on mathematical modelling and computer simulations, scientists know that if plant organs like leaves or petals are produced at regular intervals, these complex patterns can automatically emerge. So how do plants produce organs at regular intervals? Biologists knew the answer involved cells in the growing plant coordinating with their neighbours to transport the plant hormone auxin to sites where it accumulates. At each auxin hotspot, a new leaf begins to grow. But how are these hotspots formed and maintained?

Neha Bhatia, a PhD student in Marcus Heisler’s lab at EMBL, found that if a cell detects a lot of auxin, it makes neighbouring cells transport the hormone towards that cell. This creates a hotspot. At the same time, it depletes auxin levels in the surrounding area, so another hotspot can only form a fair distance away, where that cell’s influence is no longer felt. This, the EMBL scientists conclude, is what creates the regular spacing between auxin hotspots, and consequently between leaves.

Time to celebrate? Maybe not. Their experiments show the mess that occurs when the genes involved are disrupted. They engineered silent mutations in a gene named MP. The resulting plant got its spiral wrong. While that’s interesting, it doesn’t explain how normal plants get the spiral right. How does the timing and spacing conform to the Fibonacci series and the Golden Ratio? The scientists don’t talk about that. They also don’t venture to guess how it might have evolved. So while “The periodic formation of plant organs such as leaves and flowers gives rise to intricate patterns that have fascinated biologists and mathematicians alike for hundreds of years,” this team has only offered a partial explanation: a feedback mechanism that “acts broadly to generate periodic plant architectures.” Clearly, not every broadly-acting periodic process conforms to the Golden Ratio or the Fibonacci series.

We are glad for every advance in identifying processes and mechanisms in nature. But as these stories show, the most interesting questions remain unanswered: how does a natural process yield mathematically precise patterns that humans find beautiful? We all know a process that can do it: intelligence.

Watch this YouTube video of falling domino tricks. You could study the material in the dominos till the cows come home and miss the point. Sure, the dominos fall according to the Law of Gravity. The diameters of the circles affect the speed of the circuits. The angles and spacing of certain dominos follow mathematical models. But something greater is going on that cannot be explained with reference to the parts themselves. Intelligent design has the explanatory power to tackle the most interesting parts of the story. You got that by just watching the mechanism in action, even without seeing the designer set the dominos up.

Photo: Blue diadem butterfly, by Bernard Dupont [CC BY-SA 2.0], via Wikimedia Commons.