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Zoology

Colors in the wind

Genes and fossils reveal the origin of South American butterflies

ANDRÉ FREITAS/UNICAMPAgrias claudinaANDRÉ FREITAS/UNICAMP

A dinosaur decorated with the blue and red colors of a butterfly resting on its forehead, as though the butterfly were a bow tied around a little girl’s hair, might seem like a fantasy of an artist or film director shooting a prehistoric film. According to zoologist André Freitas, from the State University of Campinas (Unicamp), the image is plausible: butterflies from the nymphalid family already existed 90 million years ago.

Partnering with colleagues from Finland, Sweden, and the United States, he described, in a paper published in Proceedings of the Royal Society B, that the nymphalids were already part of the landscape when dinosaurs hunted other animals and ate the leaves of a reasonable variety of plants. In addition to being on the menu for vegetarians, it is very likely that plant variety is behind the countless forms and colors of butterflies flitting from one flower to another, suggests the researcher from Unicamp. However, both plants and animals (including butterflies) were affected by the asteroid that crashed in the region of what is nowadays Mexico, some 65 million years ago. According to this widely accepted theory on the disappearance of dinosaurs, the consequences of the impact were extremely violent, caused a massive wave of extinctions and left vestiges in the fossils and genes of today’s butterflies.

“After the massive extinctions, which occurred between the Cretaceous and Tertiary periods, only 10 Nymphalidae species survived,” says Freitas. Two figures in the article demonstrate the importance of the discovery: each one of these surviving species originated a sub-species that later diversified itself. This is why the nymphalids are divided into 12 subfamilies. After a period of time during which the world became a hostile place for most living beings, the few species that survived diversified in an explosive manner and were the origin of a wider variety of butterflies. Today, the butterfly family comprises approximately 6 thousand species of different colors and sizes. For example, butterflies can be spotted or streaked, red or blue, sometimes with eyespots that resemble big eyes.

In addition to discovering when these butterflies first appeared, the zoologist also wants to learn what region of the planet they came from and which environmental conditions were responsible for the diversity of the colors that flutter through the tropical airs. He can spend endless hours poring over a magnifying glass, examining all the details of a butterfly ? the size, colors and layout of the veins. The detailed analysis of this family considered 235 of these morphological characteristics, as well as the host plants characteristic to each subfamily, and indicates that the nymphalids first appeared in the tropics. To help establish when each species lived, the international team resorted to rare butterfly fossils, more specifically, a dozen of such fossils, whose ages were estimated by geological methods. This dating complemented the molecular models to provide a time scale for the genealogical tree of the nymphalids.

To have a more accurate idea of how and when the current variety of species appeared, it is necessary to examine this issue on a case-by-case basis. This is what Freitas has done, in collaboration with Karina Silva-Brandão, currently working as a researcher at Esalq, the Luiz de Queiroz College of Agriculture of the University of São Paulo (USP). An example is provided by the transparent wing butterflies from the Ithomiinae subfamily, which Freitas and Karina studied in partnership with France?s Marianne Elias, who was at the UK?s University of Edinburgh, at the time. The researchers published a paper in Molecular Ecology in 2009, in which they explained that these butterflies already lived in what is now the Andes Mountain Range when the region was not a mountainous one, more than 15 million years ago. As the movements of the earth?s crust formed the mountains in the western part of what is now South America, the mountain grew and new environments appeared, isolated by peaks and valleys. This was the ideal situation for the appearance of the species, which led to the diversification of the Ithomiinae. The genetic data also show that the number of species stabilized about 4 million years ago, perhaps because all the favorable environments had already been taken up.

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Some of these species were the origin for new lines in the North of the Amazon Region and in the Mata Atlântica rain forest, in regions where the plant diversity was very inviting, especially the diversity of the Solanaceae family of plants, which includes tomatoes and potatoes. Some years ago, by means of phylogenetic trees, Freitas had already shown the importance of the host plant in the diversification of the Ithomiinae. Butterfly larvae are not beings of indiscriminate voracity; when they are transported to a plant that differs from the habitual one, many of them fail to recognize the plant?s surface and starve to death, even though they are surrounded by leaves.

The ancestors of the Ithomiinae ate the leaves of the Apocinaceae, from the allamanda family, whose yellow or pink blossoms are commonly seen in gardens. When the stalks and leaves break, they spill a milky substance that is toxic to many animals. The butterfly larvae that feed on the Apocinaceae take advantage of this: they sequester the alkaloid substances and acquire an unpleasant smell that keeps predators away. This is a convenient resource, but the Apocinaceae are not enough to feed a high number of species. In view of this limitation, species would survive successfully if they could find other sources of food. “The Solanaceae were an abundant resource without any competition and this is why the access to the Solanaceae led to the diversification of the Ithomiinae,” says Freitas.

ANDRÉ FREITAS/UNICAMPFront and back: two sides of the Diaethria clymenaANDRÉ FREITAS/UNICAMP

The Acraeini was another family of nymphalids that spread from the Andes, according to a paper published by Freitas and Karina in the Molecular Phylogenetics and Evolution journal in 2008. The feeding habits seem to be very closely related to this diversification, stemming from the African butterflies specialized in eating, during the larvae stage, nettles? prickly toxin-full leaves. Researchers believe that the same capacity to adapt to the nettles led to the appearance of descendants with a preference for the sunflowers and daisy families, also rich in toxic chemical compounds. These daisy eaters also exist in South America, indicating that the subfamily had arrived in South America as descendants of the families established in the Old World.

The story goes on. Recently, Freitas and Karina describe, in an as yet unpublished paper, that the Acraeini group appeared in Africa approximately 30 million years ago. At that time, however, the American and African continents were already separated; so how did the butterflies travel from one continent to the other? “We believe they may have traveled across Antarctica,” he says. In those times, Antarctica had not yet frozen over and was covered in lush vegetation. Antarctica separated from the other continents 23 to 28 million years ago, and was surrounded by ocean currents that caused the continent to freeze. However, at that time, the Acraeini had already arrived in the New World. In addition to the information obtained from genetic analyses, the researcher from Unicamp emphasizes one more detail that supports the theory: in South America, the butterflies from this group live in cold regions, such as the Andes Mountains and the highlands of the Serra do Mar mountain range, covered by the Mata Atlântica rain forest. The African butterfly species, on the other hand, live in tropical forests and savannas. “Only the species that resisted the cold arrived here.”

Traveling
Because of strong evidence pointing to the African origin of some nymphalid butterflies, until recently, the general belief was that the Biblidinae subfamily, comprised of approximately 20 species in Africa and Asia and more than 90 species in South America, for some reason became more diversified on our side of the Atlantic Ocean. “However, this is not what we saw,” says Freitas. His analyses indicate that the Biblidinae first appeared in South America and then – approximately 30 million years ago and again 25 million years ago – invaded Africa, generating new lineages. At that time, it was no longer possible to go through Antarctica, which results in an unsolved mystery. “Perhaps an intercontinental crossing is easier than we thought,” he says, imagining that adult butterflies could have been carried by winds or traveled on natural rafts made of branches, leaves, fruit and, nowadays, of trash. It is possible that these butterflies traveled such long distances – tropical butterflies can live for up to ten months.

If a single family of butterflies has so many stories to tell, it is not difficult to imagine how many stories all 127 families of these flying insects – which also include moths – could tell. Strolls through Brazilian gardens and forests show the enormous variety of splendid butterfly colors – still greatly unexplored. According to Freitas, few researchers in Brazil focus on understanding how this diversity came about. Anyone can admire these insects in all their finery. A stroll along the trails of the Serra do Japi hills, a Mata Atlântica rain forest reserve located close to the city of Jundiaí, in São Paulo State, is breathtaking, especially in March and April.

The Project
Butterflies from the Mata Atlântica rain forest: bio-geography and systematics as tools for the conservation of biodiversity (nº 2004/05269-9); Type Young Researcher; Coordinator André Victor Lucci Freitas – Unicamp; Investment R$164,736.14

Scientific articles
Wahlberg, N. et al. Nymphalid butterflies diversify near demise at the Cretaceous/Terciary boundary. Proceedings of the Royal Society, B. v. 276, n. 1677, p. 4 295-302. 22 Dec. 2009.
Elias, M. et al. Out of the Andes: patterns of diversification in clearwing butterflies. Molecular Ecology. v. 18, n. 8, p. 1 716-29. Apr. 2009.

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