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EVOLUTION

How snakes arrived in the Galápagos

Brazilian and Ecuadorian researchers trace the routes the reptiles used to colonize the archipelago and identify three new species

Pseudalsophis dorsalis on Santa Fé Island

Miguel T. Rodrigues/USP

In November 2016, BBC One viewers were treated to a spectacular animal chase: dozens of runner snakes of the species Pseudalsophis occidentalis crawled out of crevices and attempted to capture an iguana on a beach on Fernandina, a Galápagos island 1,000 kilometers (km) off the coast of Ecuador. The iguana outruns the snakes, scaling the cliffs to a successful escape. The 2-minute, 17-second film, which won a British Academy Television Craft Award in May 2017, depicted the struggle for survival and habits of a poorly studied group of vertebrates in the archipelago—snakes.

Brazilian and Ecuadorian biologists witnessed scenes like these as they collected snakes on the Galápagos Islands, an archipelago in Ecuador comprising 13 major islands, six smaller islands, and dozens of islets and rocky outcroppings, spanning an area of 8,000 km2. Morphological (external appearance, bones, and organs) and molecular (genetic) analyses of snake specimen from the islands allowed the researchers to reconstruct their colonization routes and identify three new species. The nine recognized species are of the genus Pseudalsophis. They are between 35 and 85 centimeters (cm) in length and some occur only on specific islands of the archipelago.

The article titled “How snakes arrived in the Galápagos,” published in issue no. 270 of Pesquisa FAPESP, does not represent a public and permanent scientific record, nor does it constitute a nomenclatural act published in accordance with the guidelines of the International Code of Zoological Nomenclature (ICZN).

The common ancestor of the nine species no longer exists according to the study, which was published in August in the journal Systematics and Biodiversity. With a body length of 50 cm, P. hoodensis is thought to have been the first species derived from the hypothetical ancestor. Other species originated from it, in a process known as speciation. The ancestors of P. hoodensis must have first arrived on now-submerged islands of the Galápagos archipelago about 7 million years ago, the researchers concluded. Their conclusions are consistent with the notion that there might have been a Proto-Galápagos as proposed by American oceanographers and geologists in a 1994 article in Nature.

According to the study, the ancestors of P. hoodensis must have set out from the coast of Ecuador—where their sister species, P. elegans, is still to be found—and arrived in Galápagos on pieces of roots and branches that broke off from the shoreline. P. hoodenis is found only on Española Island—the oldest of the current string of islands—and adjacent islets. “The divergence of P. hoodensis occurred about 4.5 million years ago, initiating a process of speciation that led to the colonization of other islands by other species in the archipelago,” says biologist Hussam Zaher, a professor at the Museum of Zoology of the University of São Paulo (MZ-USP), who led the expedition.

Tribute to Darwin
Galápagos is home to many endemic species of animals: of the estimated 5,000 species inhabiting the islands, around 2,000—including birds, turtles, reptiles, and other groups—occur nowhere else. The archipelago is famous as the setting in which Charles Darwin (1809–1882) found clues that led to his formulation of the principle of natural selection and the theory of evolution in 1859. He began to wonder whether one species could originate others after seeing that turtles and birds varied in body shape between the islands he had visited in 1835 on his voyage aboard the HMS Beagle. “Darwin reported seeing a green snake on Floreana Island,” says Zaher, “but we did not find any there. They likely have become extinct.” The snakes on the islands eat birds, iguanas, smaller lizards, insects, and fish and are predated by hawks.

Of the three new Galápagos species, one was named P. darwini in tribute to Darwin. It is about 40 cm long and lives on the islet of Tortuga as well as on the larger islands of Isabela and Fernandina. Another species, which only occurs on Santiago Island and adjacent islets, was named P. hephaestus after Hephaestus, the Greek god of fire, in allusion to the archipelago’s volcanic origin. The third is P. thomasi, a species found on Santiago Island and named after American biologist Robert Thomas. A professor at Loyola University, Thomas formulated a classification of Galápagos snakes that remained in use for 20 years.

In a 1997 article in Herpetological Natural History, Thomas reclassified the four then-known species and subspecies of Galápagos snakes into three different taxonomic genera, two of which are also found on Caribbean islands. “My research on Galápagos snakes was done using data on most specimens available at museums around the world. It was entirely morphological,” says Thomas.

Two years later, in the Bulletin of the American Museum of Natural History, Zaher proposed that the species form a unique lineage more closely related to the species P. elegans of the South American west coast than to Caribbean lineages. His study was based on variation of the hemipenis—the male reproductive organ, usually located within the tail—in two species of snakes in the archipelago and in species representing South American lineages. Years later, molecular studies by his group confirmed his findings.

In a 2009 paper published in the journal Papéis Avulsos de Zoologia, Zaher and biologist Felipe Grazziotin, a researcher at Instituto Butantan, proposed a classification that better reflected these findings, integrating the Galápagos species, then considered by Thomas to be a subspecies, and the mainland species P. elegans, into a single genus called Pseudalsophis. The proposed classification was accepted by other experts.

In molecular analysis of samples collected on the expedition to the Galápagos, Grazziotin found that the species in the archipelago were related to their sister species on the coast of Ecuador and therefore must have come from the mainland. This further supported the Brazilian researchers’ hypothesis and ruled out the possibility that some species could also have come from the Antilles.

Believing that three different lineages had colonized the archipelago, Thomas had included the Galápagos snakes in the genera Philodryas, Antillophis, and Alsophis. The genus Philodryas includes aggressive species, which could indicate that the ones in the archipelago are also aggressive. However, the researchers noted that the snakes were aggressive only toward animals they prey on for food, such as iguanas. “We weren’t sure whether the Galápagos species could be aggressive or venomous like some snakes of the genus Philodryas in Brazil, but none of them attempted to bite us,” notes Grazziotin, who joined the expedition as a doctoral student under Zaher. “The most they did was defecate, a common defense behavior in this family of snakes.”

The mainland species—P. elegans—and the oldest Galápagos species—P. hoodensis and P. biserialis—average 60 cm in length. According to Zaher, this ancestral morphological pattern evolved in the archipelago, forming two distinct lineages termed as large and small insular species. The two lineages spread from east to west, cohabiting the larger islands (Santiago, Santa Cruz, Fernandina, and Isabela). Large insular species, which were 75 cm long, began to colonize the islands 3.3 million years ago, while the small species, around 25 cm long, began to occupy the younger islands 2.2 million years ago (see infographic).

Curiously, says Grazziotin, larger and smaller snakes—one species of each—can either live alone on some islands or share the same space with each other, but never with more ancient, medium-size species. “Large and small snakes can coexist without competing for food,” says Zaher. “The larger ones live on rocks and prey on adult lava lizards, young iguanas, and birds, while smaller ones can find food in more restricted environments, such as crevices in rocks, feeding on lizards and insects.”

Miguel T. Rodrigues/USP Fernandina Island, the youngest of the Galápagos IslandsMiguel T. Rodrigues/USP

The voyage
The expedition to Galápagos took place in June 2008. After the voyage came the laborious work of describing the species and performing genetic testing on collected samples, generating a wealth of information that took many years to be interpreted. Four Brazilian researchers—Zaher and Grazziotin along with Miguel Rodrigues and Luciana Lobo, both also from USP—and four Ecuadorian researchers—Yanes-Muñoz, Altamirano-Benavides, Cruz Marques, and park ranger Simon Villamar—spent two weeks at sea aboard the Queen Mabel, along with four crew members. Except for the rare nights at hotels on the larger islands, they left the boat only to collect snakes in the early morning or late afternoon.

The researchers visited 14 islands and adjacent islets, many of which are closed to visitors other than researchers, where they collected 149 specimens, of which 47 were sampled and released and the remainder were stored for detailed laboratory testing. The dominant species (44 specimens of the total) was P. occidentalis, from Fernandina Island.

The Galápagos archipelago is home to about 25,000 people, of whom 18,000 live in the city of Puerto Ayora on Santa Cruz Island. Pollution, especially plastic packaging, has been a concern for local authorities due to its potential adverse effects on wildlife. “Because of the litter,” Zaher remarked, “some islands are quite degraded.”

Project
Origin and evolution of snakes and their diversification in the neotropical region: A multidisciplinary approach (no. 2011/50206-9); Grant Mechanism Thematic Project; Program Biota FAPESP; Principal Investigator Hussam El Dine Zaher (USP); Investment R$4,921,754.91.

Scientific articles
ZAHER, H. et al. Origin and hidden diversity within the poorly known Galápagos snake radiation (Serpentes: Dipsadidae). Systematics and Biodiversity. on-line. 22 ago. 2018.
THOMAS, R. Galápagos terrestrial snakes: biogeography and systematicsHerpetological Natural History. v. 5, n. 1, p. 19-40. 1979.
ZAHER, H. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenesBulletin of the American Museum of Natural History. v. 240, p. 1–168. 1999.
ZAHER, Hussam et alMolecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia. v. 49, n. 11, p.115-3. 2009.
CHRISTIE, D. M. et alDrowned islands downstream from the Galapagos hotspot imply extended speciation timesNature. v. 355, p. 246-8. 16 jan. 1992.

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