Evasive butterfly mimicry reveals a supercharged biodiversity feedback loop

Key points

• Scientists constructed a family tree for butterflies in the genus Adelpha, which are native to North and South America and display perplexing color patterns that may represent an unusual case of evasive mimicry.
• They found the first known correlation between latitude and the rate of mimicry evolution in butterflies, consistent with a longstanding theory of biodiversity that can trace its origin to Alfred Russel Wallace, the co-discoverer of evolution by natural selection.
• The tree helps reconstruct the evolution of mimicry in Adelpha butterflies through their 25 million-year history and lead to the establishment of a new genus of butterflies in South America.

In the early 1990s, Keith Willmott and a friend, both undergraduate students from the United Kingdom, arrived in Ecuador with impressionable minds and big aspirations.

“We had a long-term goal to write a series of field guides on the butterflies of Ecuador. We didn’t realize how long-term a goal it was at the time, because we’re still working on them,” said Willmott, now a curator of Lepidoptera at the Florida Museum of Natural History. He initially imagined there might be 20 to 30 butterfly species in the region that had yet to be described; once those had been named, writing the field guides would be a mere matter of taking a few photos and spelling out where everything lived.

But, as Willmott noted, they were “hopelessly inaccurate” in their estimates. More than 30 years later, Willmott, his friend, their colleagues and other researchers have described more than 300 new butterfly species native to Ecuador, with no end in sight.

Among Ecuador’s many butterflies, one group in particular has been a source of consternation. Seven years before Willmott first set foot in the Ecuador, Annette Aiello of the Smithsonian Tropical Research Institute wrote: “For the past century, Lepidopterists have puzzled over the genus Adelpha…in an attempt to discover the secret character or combination of characters which might lead to a satisfying classification of the 100 or more butterfly species included in this large, neotropical genus. The result has been a hopeless tangle.”

There’s still a significant amount of work that needs to be done on the long-anticipated field guides, but with the publication of a new study in the journal Systematic Entomology, Willmott and his colleagues have largely untangled the Gordian knot of relationships among species in Adelpha, with the exception of a few persistent kinks here and there. Along the way, the study authors also gathered support for a longstanding theory of biodiversity that may explain why there are more species in the tropics than there are in temperate regions.

Adelpha may display a rare or overlooked type of mimicry

One of the primary difficulties confronted by those who study Adelpha butterflies is their appearance. Individuals within the same species sometimes look strikingly different, while two species that may only share a distant relationship can look nearly identical. Thus, any attempt to sort out Adelpha relationships based on superficial appearance inevitably leads to a dead end.

Then there’s the question of why they look the way they do. “It’s long been thought that there’s maybe some mimicry going on in the genus, but they are a very atypical group in terms of what you would expect from mimetic butterflies. They don’t seem, to me, to be obviously chemically protected,” Willmott said.

Many butterflies that mimic each other accumulate toxins in their bodies from the plants they consume during their larval stage, which makes them unpalatable to birds and other predators. But in several studies in which researchers presented what were thought to be toxic Adelpha butterflies to birds, the birds often showed no compunction whatsoever and eagerly chowed down on the proffered meal. Instead, some researchers think their mimicry might be based on speed and unpredictability.

“They have an erratic flight with sharp dives, and they can change direction very rapidly,” said lead author Erika Páez, who conducted the research while working toward a doctoral degree at the L’Institut de Systématique, Évolution, Biodiversité.

This type of mimicry is currently considered rare and has only been proposed to exist in a handful of animal groups. This includes a case of lookalike butterflies in South Africa, certain flea beetles that catapult themselves away from predators and their ground beetle doppelgangers that can’t jump, and a group of ponderous weevils that look like swift-moving flies.

Willmott and colleagues think that Adelpha butterflies are engaged in something called Müllerian mimicry, a sort of strength-in-numbers approach in which all species with a desirable trait look the same.

If you were “it” in a game of tag, and one of your competitors was an Olympian speed runner, you’d quickly conclude that your time would be best spent chasing after some of the slower players. If there were multiple Olympian runners in the group, they’d save a lot of energy if they all wore the same uniform, implicitly telling you not to bother trying to catch any of them.

This is more or less what seems to be happening in Adelpha.

In a separate study, Páez designed an experiment to test this idea. In the experiment, whenever a bird moved to pounce on a butterfly (in this case, a piece of paper the shape and color of an Adelpha tied to a string), Páez yanked the butterfly away, leaving behind an agitated bird with an empty stomach. When she repeated the experiment, the same bird might fall for the ruse a few more times, but it’d quickly learn it wasn’t worth the effort and lose interest in attacking anything that looked like an Adelpha. This was so effective, in fact, that birds learned to avoid the fast “butterflies” in less time than it took them to avoid those that were genuinely unpalatable (an identical paper butterfly that was soaked in a bitter-tasting compound).

Many Adelpha species have large geographic ranges that span the American tropics. When viewed at this scale, there are three mimicry patterns that account for most of the diversity in the genus, each named for a butterfly that bears markings typical of the respective pattern.

In the first, called COCALA, butterflies have dark amber wings with two highly contrasted beams of white that originate near the base of the hindwings and fan out at a 45-degree angle like searchlights, and two smoldering flame-colored bands of equal size across the forewings.

In the second group, called IPHICLUS, the white bands span much of the fore- and hindwings, and the orange scales are reduced to small spots. In the third, SALMONEUS, only oblique orange bands are present.

Adelpha butterflies that evolve and adhere to one of these patterns presumably have a better chance of getting through the day without being eaten, which accounts for the fact that even distantly related species can look alike.

There are also variations of these general color schemes at smaller scales. In the Apure region of Venezuela, seven species appear to have independently evolved a second orange band on their hindwings. Outside of this region, these same species lack the additional band.

The three main mimicry patterns can be conceived of as a strong evolutionary current sweeping Adelpha butterflies along through time and keeping them together. The more localized patterns, such as the one in the Apure region, are like the various eddies and gyres that form within a larger current — all still traveling in the same direction, but with their own distinct shapes and rotations.

Adelpha mimicry might demonstrate biodiversity feedback loop

Not all Adelpha butterflies are mimics. Species in the genus can be found as far south as Argentina and as far north as the United States, with a terminal distribution in Colorado and Nevada. Those in North America seem to have a lower rate of mimicry evolution than species in South America.

Taken at face value, this seems to support a theory that helps explain why the tropics are exponentially more diverse than temperate regions.

Take trees, for example, of which there are about 700 species in North America. In Ecuador, in a plot of land smaller than Hawaii’s smallest island, there are more than a thousand, and in the whole of tropical South America, there are at least 22,000 tree species.

Biologists get positively giddy when they encounter natural phenomena of this scale and complexity, and starting with Alfred Russel Wallace (who independently developed the theory of evolution by natural selection at the same time as Charles Darwin), they’ve put forward several plausible theories to explain it.

Wallace thought it may have had something to do with ice ages, given that glaciers during the recent Pleistocene epoch stretched nearly all the way down to Tennessee in North America, rendering large swaths of land uninhabitable and resulting in a wave of extinctions. In contrast, he wrote: “equatorial lands must always have remained thronged with life. In one, evolution has had a fair chance; in the other it has had countless difficulties thrown in its way.” Wallace may have been right, but paleontologists have since learned that the tropics were more diverse than temperate regions long before the Pleistocene, so there must be other factors at play.

According to another theory, high temperatures result in faster rates of genetic mutation, which in turn speeds up diversification. This might make sense for organisms like plants that assume the ambient temperature of their surroundings, but it doesn’t account for animals that generate their own heat and maintain a constant body temperature, like mammals. So, if true, this isn’t the whole story either.  

A third theory with a little more traction and explanatory power states that diversity in the tropics is highly influenced by the interactions among species. In this view, stable habitats — including many tropical regions, where seasonal changes are less pronounced than temperate regions — can support a greater number of species. This process creates a sort of diversification feedback loop, in which a greater number of species leads to increasingly complex interactions among them, further spurring diversification and the evolution of new traits.

We have Wallace to thank for this idea as well. In the same sentence in which he mentions glaciers, he adds that equatorial lands “have been unintermittingly subject to those complex influences of organism upon organism, which seem the main agents in developing the greatest variety of forms and filling up every vacant place in nature.”

In the case of mimicry, that might look something like a greater number and variety of predators in an ecosystem, which increases the amount of pressure on butterflies to look a certain way.

Scientists tackled three Adelpha mysteries

There’s very little that can be inferred about the evolution of mimicry without first having a robust family tree to understand how species are related. Prior to this study, it remained unclear how many Adelpha species really did independently evolve the same color patterns or if they looked similar because they’re closely related and inherited their color pattern from an ancestor.

It would also be impossible to say whether the preponderance of mimicry in the tropics was caused by a runaway train of biotic interactions or simply a fluke of there being more Adelpha species in the tropics than there are at higher latitudes.

These are the first two questions the authors set out to answer in their study.

It goes without saying that simpler, more practical questions like “how many Adelpha species are there, anyway?” and “are any of them in danger of going extinct?” are impossible to answer without a firm understanding of their relationships.

To find this out, the study authors extracted and sequenced DNA and RNA from museum specimens. They combined this with DNA sequences used in previous studies, leaving them with data for 83 of the 87 putative species of Adelpha.

This is somewhat less than the “100 or more butterfly species” estimated to exist by Aiello in her 1984 study on Adelpha that preceded Willmott’s initial trip to Ecuador. Given the difficulty of identifying Adelpha species based on their looks, it makes sense that butterflies thought to represent multiple species would occasionally be found to represent only one.

There’s also a group of six species that look like other Adelpha butterflies but can’t seem to make their mind up about which family reunion to attend. All of them live on upper mountain slopes in Central and South America, where clouds run aground and obscure the stunted forests in a near-perpetual haze. But a study published in 2022 suggested that these species actually should be placed in a genus of butterflies called Limenitis, whose species are primarily native to northern more temperate regions.

These six are unusual in that they lay their eggs on plants in the honeysuckle family. And while other Adelpha may not like honeysuckle, it’s a staple among Limenitis butterflies, which commonly eat honeysuckle plants as caterpillars.

Páez, Willmott and their colleagues were particularly interested in figuring out what was going on in this group, constituting the third question that needed answering. 

By combining and analyzing their data, the authors reconstructed the Adelpha family tree, which they then used to address these questions.

First, they showed that the IPHICLUS wing pattern — the one with the longer white bands and the two residual splashes of orange — is likely the oldest pattern in the genus and that it evolved more than 20 million years ago in the ancestors of modern Adelpha. The pattern changed during the intervening eons, at times disappearing altogether in some species only to reappear millions of years later. Living species that sport this pattern are typically close relatives, meaning it’s unlikely IPHICLUS evolved independently in different groups but was instead passed down through inheritance.

In contrast, the two other common color schemes — COCALA and SALMONEUS — adorn the wings of butterflies that generally bear no close relation to each other, indicating they’ve evolved the pattern multiple times in response to predation or other selective pressures.

The authors also confirmed that the rate of mimicry pattern evolution really was higher in tropical Adelpha. According to study co-author Marianne Elias, director of research at the French National Center for Scientific Research, “this means that new patterns are produced more often in the tropics.”

“In equatorial regions, it seems like the rate of mimicry evolution is faster,” Willmott said. “To our knowledge, it’s the first time that a link between the evolution of a mimicry color pattern and latitude has been demonstrated.”

It’s also another compelling piece of evidence that biodiversity on our planet grows in size and complexity the more it interacts with itself.

Finally, they reached a sort of compromise concerning the strange group of Andean butterflies with dueling affinities for the genera Adelpha and Limenitis. The conclusion they came to is that the Andean butterflies cannot be placed convincingly in either group. Instead, they constitute what the authors consider to be a new genus of butterflies, which they named Adelphina.

There’s much left to learn about this small segment of Earth’s insect diversity. For starters, scientists know practically nothing about the mating habits of Adelpha butterflies, primarily because the females rarely venture close enough for anyone to study them. Both males and females “almost always fly in the canopy of the forest, but only the males descend to search for minerals, which they likely transfer to females when they are mating. That’s why females are very rare in museum collections,” Páez said.

It’ll also take more research for scientists to feel fully confident in saying that Adelpha mimicry is really driven by evasiveness rather than unpalatability. It’s possible that both types of mimicry are present in this group.

Study authors additionally include Gael Kergoat of the Centre de Biologie pour la Gestion des Populations; Nicolas Chazot of the Swedish University of Agricultural Sciences; Mohamed Benmesbah; Adriana Briscoe of the University of California; Susan Finkbeiner of California State University; André Freitas and Luiza Moraes Magaldi of the Universidade Estadual de Campinas; Robert Guralnick, Ichiro Nakamura and Maxwell Woodbury of the Florida Museum of Natural History; Ryan Hill of the University of the Pacific; Marcus Kronforst of the University of Chicago; Sean Mullen of Boston University; Hannah Owens of the University of Florida; and Niklas Wahlberg of Lund University.

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