Animals

Some Butterflies Have Been Fooling Others for 2 Million Years

Research on butterfly mimicry sheds light on how the evolution of beneficial traits can come with unexpected — and undesired — consequences.

Several different swallowtail butterfly variations showing mimicry and polymorphism, or different forms of the same species. In the center, a female Papilio polytes that mimics another species, which is toxic to predators. | Matt Wood, University of Chicago
Several different swallowtail butterfly variations showing mimicry and polymorphism, or different forms of the same species. In the center, a female Papilio polytes that mimics another species, which is toxic to predators. | Matt Wood, University of Chicago

Red-bodied swallowtail butterflies look so delicate and beautiful that their discoverers named them after flower colors, such as crimson rose. But these eye-catching insects are more sinister than one might imagine.

If an unfortunate predator — even a human — decides to eat one, gagging and severe vomiting may follow. The aftermath is so miserable that victims rarely prey on the butterflies again.

The common Mormon swallowtail butterfly (Papilio polytes), conversely, tastes delicious to birds and other predators. That poses survival challenges for the insects, so females of the species have evolved the ability to look just like toxic red-bodied swallowtails.

Female common Mormons sport different colors, patches, and patterns, though, and only some mimic red-bodied swallowtails. This multi-form phenomenon reminded early entomologists of Mormons who historically practiced polygamy, whereby men may have several wives.

New research on common Mormons and other butterflies published in the journal Nature Communications finds that some populations of these insects have maintained multiple female forms — including mimics — for millions of years.

Understanding the genetic processes that led to these imposters could facilitate research on what are known as “sex-limited” traits and diseases in humans. This means that the conditions tend to affect one sex more than the other.

Lead author Wei Zhang of the University of Chicago’s department of ecology and evolution said the research helps to address classic evolutionary questions and better understand sex-limited traits and diseases in other organisms.

“As far as we know, sex-limited traits and diseases widely exist in many sexually reproducing species as well as in humans, such as baldness and red-green color blindness,” she said.

Common rose swallowtail butterfly | Wikimedia Commons

In a prior study, Zhang, senior author Marcus Kronforst, and their team determined that the entire sex-limited mimicry phenomenon in common Mormons and other butterflies is controlled by a single gene named doublesex.

“The doublesex gene is involved in the sex determination of many insects and it gains additional duty in controlling mimicry in some Papilio butterflies,” Zhang said.

The gene actually inverted, or flipped, about 2 million years ago, with this topsy-turvy version dictating wing patterns in females. Doublesex is classified as being a supergene, which usually refers to groups of several tightly linked genes that are inherited together. In this case, however, the supergene is a single multi-tasking gene and not a group.

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For the new study, the researchers reconstructed the evolutionary history of the doublesex gene by analyzing whole-genome sequence data from common Mormon butterflies and several similar species to see how they are related to each other and how their copies of the gene compare.

The scientists shared that the most closely related species to the common Mormon butterfly, spangle, is spread across mainland Asia from India to Japan and did not develop mimicry. In this species, both males and females look alike.

Other swallowtail species that spread from the mainland to islands in the Philippines and Indonesia developed three or four distinct forms, a feature known as polymorphism. Other swallowtails spread further into Papua New Guinea and the northeast coast of Australia. But females within those species display only one disguised wing pattern.

Several different swallowtail butterfly variations showing mimicry and polymorphism, or different forms of the same species. Row 1: A female and male Papilio protenor, the species that is closely related to Papilo polytes, the focal of the new study. In P. protenor, males and female look the same and they do not mimic. Row 2: Papilio ambrax, a species where males and females look different and the female is a mimic. In this species, there is no female polymorphism. The new study shows that its evolutionary ancestor was polymorphic, but females lost that trait and only display the mimetic form. Row 3: Polymorphic Papilio polytes, (L-R) A mimetic female form (one of 3 mimetic forms in this species), a non-mimetic female, and the male. Row 4: A distantly related swallowtail, Pachliopta aristolochiae. This is the toxic species that the species in the new study mimic. | Matt Wood, University of Chicago

The researchers attempted to match the patterns they saw in the genome sequence data to possible explanations for how mimicry developed over time and place in the various butterflies. The evidence supports that once the doublesex gene flipped, a process called balancing selection occurred.

Kronforst said if one mimetic color pattern becomes too common in a population, predators learn that it is palatable because they frequently encounter the mimic and not the toxic model.

“The process can cause the mimetic species to evolve to match multiple models, leading to polymorphism,” he said.

Models, in this case, refer to species that the imposter is mimicking.

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Zhang added that various wing forms can also result from members of the same species being geographically widespread, leading insects to mimic different local toxic butterflies.

The researchers observed some butterfly populations maintaining multiple female forms for millions of years, while others lost their original, undisguised form. Historically, the smallest butterfly groups, such as the ones that spread to Australia, lost the polymorphism, allowing genetic drift — essentially genetic variation due to chance — and natural selection to weed out the original form.

Common Mormon female butterfly | Jeevan Jose, Wikimedia Commons

The findings reveal the surprising role of chance in both the spread and loss of a beneficial trait, which for certain swallowtails is the mimicry of poisonous butterflies. They also show how powerful a single gene can be.

While humans do not have a doublesex gene, we have numerous other supergenes.

“The supergenes exist in many animals and plants,” Zhang explained. “For example, the human major histocompatibility complex (MHC) contains a group of tightly-linked genes that are functionally related and play roles in the human immune system.”

The basic laws of genetics underlying the evolution of doublesex and MHC supergenes are the same. Understanding these processes can shed light on the evolution of not just beneficial traits, but also deleterious ones.

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Regarding common Mormons, Kronforst said, “We think a bunch of differences were accidentally captured when one copy of the gene flipped and became the mimetic copy. Because a lot of those changes are functional, they could be detrimental to health.”

In fact, some research shows that butterfly female mimics do not live as long as standard ones. The flipped doublesex gene may not be recombined with the original version, leading to both good and bad consequences.

It could be that the genes associated with undesired sex-specific traits in humans, such as male pattern baldness, confer some unknown benefits to those who harbor the genes.

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