Scientists publish largest-ever molecular phylogeny of a family that includes lancehead pit vipers and rattlesnakes, extending knowledge regarding the origin and diversification of these species (photo: Bothrops insularis, the Golden lancehead, on Queimada Grande Island in São Paulo State / Daniela Gennari)

Research highlights diversification in vipers
2017-03-15

Scientists publish largest-ever molecular phylogeny of a family that includes lancehead pit vipers and rattlesnakes, extending knowledge regarding the origin and diversification of these species.

Research highlights diversification in vipers

Scientists publish largest-ever molecular phylogeny of a family that includes lancehead pit vipers and rattlesnakes, extending knowledge regarding the origin and diversification of these species.

2017-03-15

Scientists publish largest-ever molecular phylogeny of a family that includes lancehead pit vipers and rattlesnakes, extending knowledge regarding the origin and diversification of these species (photo: Bothrops insularis, the Golden lancehead, on Queimada Grande Island in São Paulo State / Daniela Gennari)

 

By Peter Moon  |  Agência FAPESP – Sixty-three of Brazil’s 392 known snake species are venomous. These species are divided into four families. The family Viperidae is represented in Brazil by 30 species of Bothrops lancehead pit vipers, including B. jararaca, B. jararacussu and B. urutu, and rattlesnakes including Crotalus durissus.

The family Viperidae is not exclusive to South America. Viperids are among the most successful venomous snakes in evolutionary terms, with 329 known species inhabiting almost every continent. They are believed to have originated in Asia or Africa and to have migrated later to the Americas. Recently, scientists have begun to elucidate when this occurred and the dynamics of this diversification.

An extensive molecular study establishing the most detailed phylogeny of the family Viperidae to date has recently been published in the journal Molecular Phylogenetics and Evolution.

The first author is Laura Rodrigues Vieira de Alencar, a postdoctoral fellow at the University of São Paulo’s Bioscience Institute (IB-USP) in Brazil. The other authors are Tiago Quental and Marcio Martins, professors in the Ecology Department at IB-USP; Felipe Grazziotin and Hussam Zaher, researchers at the same university’s Zoology Museum (MZ-USP); and scientists affiliated with the University of California, Los Angeles (UCLA).

“To understand the evolutionary history of Viperidae, we had to obtain a more robust and complete phylogeny in terms of both the number of species and the genes. Using this new phylogeny, we could then work out diversification patterns and establish dates for the main divergence events relating to lineages of Viperidae,” Alencar said.

The authors used the fossil record in combination with molecular data and statistical models to estimate the dates of species separation events. 

The new phylogenetic analysis was based on molecular data for 263 species, corresponding to 79% of all living members of the family Viperidae. All three subfamilies were covered, Viperinae (71 of 98 living species), Crotalinae (191 of 232) and Azemiopinae (1 of 2), and all but one of the genera included in these subfamilies.

The survey also included molecular data for 97 species belonging to 11 other families. This mountain of data was analyzed from the standpoint of 11 genetic markers located in both mitochondrial and nuclear DNA.

“The main challenge was to combine in a single analysis all the data generated by several researchers around the world,” said Grazziotin, one of those responsible for the genetic analysis.

Some of the DNA sequences were obtained by the researchers themselves, whereas others were obtained online from GenBank, a public database maintained by the US National Center for Biotechnology Information (NCBI), and BOLD, maintained by the International Barcode of Life Project (iBOL).

“We performed a thorough information-mining process, taking care to use only reliable data,” Grazziotin said. “The challenge was to construct a molecular matrix as a basis for the entire analysis.”

The study was supported by FAPESP as part of the Thematic Project “Origin and evolution of snakes and their diversification in the Neotropics: a multidisciplinary approach”, with Zaher as principal investigator.

Ancestral divergence 

The fossil record used in the study includes Haasiophis terrasanctus, which lived in the Middle East almost 100 million years ago, as well as Titanoboa cerrejonensis, the largest snake analyzed, at up to 13 meters – remains of this giant boa found in Colombia have been dated to 57 million years ago. The study also used data for species that lived in India, the United States and Germany during the Eocene and Miocene, between 55 and 23 million years ago.

“We made a strong effort to date the phylogenetic relationships we found but always maintained a conservative approach, taking into account the doubts about the position of the fossils used to calibrate the analysis and the uncertainties regarding tree topology,” Grazziotin said.

The datings entailed a considerable margin of uncertainty. However, this was not because only 11 molecular markers were used, as a larger number of markers would not necessarily have improved the dating confidence interval.

“It is very difficult to know whether the result would be more accurate, or even different, with a larger number of loci,” Grazziotin said. A genetic locus is the position of a gene or genetic marker on a chromosome. 

“Genomic studies with hundreds of loci have shown that some kinship relations among organisms are really hard to resolve even when you are analyzing almost the entire genome.”

The datings in the new phylogeny suggest that the ancestral divergence of viperids from their sibling group occurred some 64.5 million years ago, during the Paleocene.

This was immediately after the mass extinction at the end of the Cretaceous, some 66 million years ago, wiped out some 70% of all plant and animal species, including the dinosaurs. The data suggest that members of Viperidae are descendants of a species that survived that extinction event.

The datings also show that the ancestral species of the family Viperidae began to diversify into new lineages between the end of the Paleocene and the middle of the Eocene, some 59.9-40.4 million years ago.

The subfamilies Viperinae and Crotalinae emerged between the middle of the Miocene and the late Oligocene, approximately 49.9-28.3 million years ago. Until then, the evolution of Viperidae was confined to the Old World. It was only in the transition from the Oligocene to the Miocene that the first vipers migrated to the New World, approximately 31.0-20.9 million years ago.

Once there, these vipers rapidly diversified and radiated geographically, occupying all the main ecological niches available, of which there were many. Speciation rates then slowed down, remaining slower until the present time.

“We expected to observe a change in diversification dynamics at the point of emergence of the subfamily Crotalinae, the only subfamily with loreal pits, which are heat-sensitive organs on each side of the head between the eye and nostril,” Alencar stated.

These organs detect heat changes in the external environment, helping pit vipers locate prey, avoid predators and find sites to maintain thermoregulation. Snakes are cold-blooded animals and need to bask in the sun for a few hours each day to raise their internal temperature and accelerate their metabolism before, for example, hunting for prey.

“Loreal pits give these snakes an adaptive advantage over other subfamilies. We thought the emergence of this organ must have triggered rapid diversification of the subfamily, but that was not what we discovered,” Alencar said.

“Actually there was a change in the diversification pattern, except that it occurred not when the loreal pit developed but a few million years later. Apparently, evolution of the loreal pit was not sufficient to stimulate diversification. Other factors must also have contributed, such as the expansion of forest cover in East Asia and the invasion of the New World.”

Quental explained that the research group is now investigating how the evolution of arboreality may have influenced speciation rates and morphological diversification in Viperidae.

“Our findings suggest that the evolution of arboreality led to more limited morphological diversification, whereas terrestrial lineages display greater morphological variation,” he said. “Nonetheless, the speciation rates of arboreal and terrestrial lineages were similar, which suggests that the morphological limitations imposed by arboreality did not affect the dynamics of species diversification.”

Members of the family Viperidae account for more than 90% of accidents involving venomous snakes in Brazil. The various species of the family Elapidae, especially coral snakes, account for the remainder.

The article “Diversification in vipers: phylogenetic relationships, time of divergence and shifts in speciation rates” (doi: http://dx.doi.org/10.1016/j.ympev.2016.07.029) by Laura R.V. Alencar, Tiago B. Quental, Felipe G. Grazziotin, Michael L. Alfaro, Marcio Martins, Mericien Venzon and Hussam Zaher can be retrieved from sciencedirect.com/science/article/pii/S105579031630185.

 

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