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Supergene Discovered in Lookalike Butterflies

A butterfly’s varied disguises are controlled by variants of a single gene, partially confirming—and refuting—a decades-old hypothesis.

By | March 5, 2014

Common Mormon butterfly WIKIPEDIA, MUHAMMAD MAHDI KARIMFemale Common Mormon butterflies (Papilio polytes) are a varied lot. Some look like the black-and-white males, but others mimic the more colorful toxic swallowtail butterflies to fool predators into thinking that they are similarly distasteful.

The mimetic females come in three distinct patterns and, for decades, scientists believed that these different disguises were controlled by a “supergene”—a cluster of genes that each control different parts of the wings, but are inherited as a single block.

But Krushnamegh Kunte from the Tata Institute of Fundamental Research in Mumbai, India, has now shown that the supposed supergene is, in fact, a single gene called doublesex. By expressing different versions of the gene at different levels, the butterflies can radically switch their wing patterns to mimic many different species. Kunte’s results are published today (March 5) in Nature.

The doublesex discovery is doubly surprising because this gene already has a well-defined role: it sends developing butterflies down either a male or female path. “Finding a single gene was a surprise,” said Kunte. “That it’s such a well-characterized gene with a completely different function is totally mind-boggling.”

British scientists Sir Cyril Clarke and Philip Sheppard came up with the supergene idea in 1960s, after their cross-breeding experiments showed that Common Mormons inherit their entire wing patterns as one, rather than as separate elements. The concept has since been very influential, although no one had actually identified the clustered genes.

Kunte, together with Marcus Kronforst at the University of Chicago and their colleagues, finally achieved this by comparing non-mimetic females that resemble males with those that look like the common rose swallowtail. They searched for parts of the butterfly’s genome that were linked to the mimetic patterns, and eventually identified a small region containing five genes. Four of these were similar in all the females, regardless of their patterns.

But the fifth gene—doublesex—differed between the mimetic and non-mimetic females at more than 1,000 nucleotides. “It was a hotspot of molecular evolution,” said Kunte. “If you look at flies or beetles, this gene is very conserved. Only in mimetic and non-mimetic females of this one species do you see such diversity.”

These mutations change the way the doublesex protein folds. However, they do not affect the parts of the gene involved in separating the sexes, allowing it to retain its usual function while picking up a new role as a wing-pattern controller.

Kunte and Kronforst also found that when doublesex is transcribed into RNA, the transcript is spliced into four distinct forms—three found in females, and one in males. It appeared these forms would explain the females’ varying disguises, but every female carries all three isoforms regardless of its colors. Instead, it’s the gene’s expression that matters. The team showed that doublesex is more strongly expressed in the mimetic females, and in parts of the wing that produce white markings.

Although doublesex is just a single gene, it still fits with the classical concept that Clarke and Sheppard proposed. Kunte and Kronforst found that the mimetic version of doublesex is inverted relative to the non-mimetic one, so it sits in a different orientation in the genome. This stops the different alleles from shuffling with one another, and ensures that their thousand mutations are all inherited together.

Rather than a cluster of tightly linked genes, doublesex is a cluster of tightly linked mutations in a single gene.  As Mark Scriber from Montana State University told The Scientist in an e-mail, it is “truly amazing” that Clarke arrived at roughly the right answer 60 years ago, without having access to any modern molecular techniques.

Other scientists have discovered classical supergenes in many other organisms, including other butterflies. For example, Matthieu Joron from the French National Centre for Scientific Research showed that the varied patterns of Heliconius butterflies are controlled by clusters of many genes, which are also locked together by a genomic inversion. “The two lineages independently evolved a remarkably similar solution in response to similar pressures for precise mimicry,” he wrote in an e-mail. Joron added that he would now like to know what each element in the Common Mormon doublesex gene does, and why they need to be kept together to produce the full mimetic patterns.

Kunte also wonders whether scientists have typecast doublesex as a sexual differentiation gene, when it could potentially do much more. “Throughout the animal kingdom, you see tremendously different males and females,” he said. “Maybe this particular gene family, involved in sex determination throughout the animal kingdom, is also involved in making deer antlers or peacock tails.”

K. Kunte et al., “doublesex is a mimicry supergene,” Nature, doi:10.1038/nature13112, 2014.

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Avatar of: CharlieB

CharlieB

Posts: 1

March 5, 2014

But the first authors are Kunte and ZHANG, not Kunte and Kronforst! Why are you leaving Zhang out of the picture, Ed Yong? 

Avatar of: Woodruff

Woodruff

Posts: 1

March 6, 2014

The definition of a supergene is a group of genes that evolve together because they are within an inversion.  Why is doublesex then considered a supergene?

Avatar of: James V. Kohl

James V. Kohl

Posts: 156

March 6, 2014

Re: "Maybe this particular gene family, involved in sex determination throughout the animal kingdom, is also involved in making deer antlers or peacock tails."

My comment: That seems to be biologically plausible. One gene family and biophysically constrained chromosomal rearrangements could be involved at the advent of sexual reproduction in unicellular organisms and also in determination of the morphological and behavioral phenotypes of all other species that sexually reproduce. That idea was unknowingly suggested in the context of Darwin's "conditions of life."

Dobzhanksy (1972) extended Darwin's ideas about 'conditions of life' to flies. We extended the idea that 'conditions of life' are nutrient-dependent and pheromone-controlled in flies and all species from yeasts to mammals in a 1996 review article From Fertilization to Adult Sexual Behavior.

Others extended our model of genetically-predisposed epigenetically-effected conserved molecular mechanisms that link the epigenetic landscape to the physical landscape of DNA in organized genomes to life history transitions in honeybees via hormone-organized and hormone-activated differences in insects,

We wrote: "Small intranuclear proteins also participate in generating alternative splicing techniques of pre-mRNA and, by this mechanism, contribute to sexual differentiation in at least two species, Drosophila melanogaster and Caenorhabditis elegans... That similar proteins perform functions in humans suggests the possibility that some human sex differences may arise from alternative splicings of otherwise identical genes (p. 337)."

Most people ignored the idea that the conserved molecular mechanisms we detailed in our section on molecular epigenetics might link Darwin's 'conditions of life' to sexual reproduction in all species that sexually reproduce. Even now, the focus seems to be on what constraint-breaking mutations might do, in theory.

What Kunte et al. (2014) have shown appears to add more experimental evidence that refutes theories based on population genetics. The experimental evidence supports the likelihood that biophysical constraints on ecological variations and ecological adaptations underlie species diversity. That representation is consistent with what was recently expressed in Physiology is rocking the foundations of evolutionary biology.

In my model, for example, the physiology of reproduction and species diversification is biophysically constrained because it is nutrient-dependent and pheromone-controlled. That biological fact suggests the differences between mimetic and non-mimetic females at more than 1,000 nucleotides is not due to a thousand mutations that are inherited together. Instead, Kunte et al. (2014) appears to confirm the biological fact that the differences are nutrient-dependent and pheromone-controlled. That fact enables the expression of differences in ever-changing ecologies.

The changing ecologies appear to drive species diversity, but only in the context of biophysically constrained protein folding in species from microbes to man. Is it biologically plausible for mutations to do what food odors and pheromones do in butterflies and other species? Is there a model for that, or is it still just an idea based on population genetics?

Avatar of: N K Mishra

N K Mishra

Posts: 21

March 6, 2014

"Doublesex " is used a noun or an adjective?

Replied to a comment from CharlieB made on March 5, 2014

March 8, 2014

Most likely, Zhang is a colleague of either Junte or Kronforst.  I think Ed Yong was trying to point out that the work was a collaboration between two groups in different institutions in different parts of the world, one headed by Kunte and the other headed by Kronforst.  

Avatar of: James V. Kohl

James V. Kohl

Posts: 156

Replied to a comment from James V. Kohl made on March 6, 2014

March 11, 2014

Biologists zero in on role of plasticity in evolution

Excerpt: "...were able to show that a single molecular pathway plays a role in both heritable changes in the flies' number of ovarioles—egg-producing compartments in the ovaries—and in how they react to their environments by shutting down some ovarioles."

This experimental evidence also supports the claim that ecological variation in nutrient availability controls ecological adaptations via the metabolism of nutrients to species-specific pheromones. Effects of food "odors" and pheromones link the epigenetic landscape to the physical landscape of DNA in the organized genomes of species from microbes to man via conserved molecular mechanisms, not via mutations.

See also: Human pheromones and food odors: epigenetic influences on the socioaffective nature of evolved behaviors

Avatar of: Roy Niles

Roy Niles

Posts: 57

Replied to a comment from James V. Kohl made on March 6, 2014

March 11, 2014

Here's old Kohl again pretending to be a scientist so he can continue selling the perfumes that he also manufactures.  Nutrient dependant and pheremone controlled?  Baloney.  Pheremones are signals, not signalers.  You might otherwize want to claim your bowel movements are controlled by an emssion of gas from thr anus.

Avatar of: James V. Kohl

James V. Kohl

Posts: 156

Replied to a comment from Roy Niles made on March 11, 2014

March 18, 2014

Thanks Roy,

It's always great to hear from someone who is convinced that conserved molecular mechanisms do not link nutrient-dependent pheromone-controlled ecological adaptations in species from microbes to man.

However, it's becoming more difficult not to laugh at your ignorance after senior author Sean B. Carroll published: A Single Gene Affects Both Ecological Divergence and Mate Choice in Drosophila. The single gene is, of course, epigenetically-effected by nutrients associated with food odors and by pheromones that control the physiology of reproduction.

Thus, his comments in Evolutionary biology: Sex, lies and butterflies, which attribute mimicry to mutations and natural selection via predation, clearly represent what you've been taught to believe  -- without question -- about mutation-driven evolution. It is neither biologically plausible nor ecologically validated in any species, yet you believe in it.  And you comment here as if there was something known to you about biologically based cause and effect across species that was not common to flies and butterflies.

Instead, you shoud comment on Sean B. Carroll's representation of how ecological variation leads to ecological adaptations in flies but not in butterflies.

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