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Hitting snooze on the molecular clock: rabies evolves slower in hibernating bats

May. 17, 2012

Writer: Beth Gavrilles, bethgav@uga.edu

Contact: Daniel Streicker, dstrike@uga.edu


The rate at which rabies virus evolves in bats may depend heavily upon the ecological traits of its hosts, according to researchers at the University of Georgia, the U.S. Centers for Disease Control and Prevention, and KU Leuven in Belgium. Their study, just published in the journal PLoS Pathogens, found that the host’s geographical location was the most accurate predictor of the viral rate of evolution. They found that rabies viruses in tropical and sub-tropical bat species evolved nearly four times faster than viral variants in bats in temperate regions.

Evolutionary biologists have long recognized that molecular evolution proceeds in a largely clock-like manner, with mutations accumulating at a fairly constant rate over time. This ‘molecular clock’ allows for powerful inferences, from dating the origins of species to the origins of epidemics. However, the rate at which the clock ticks varies dramatically among species and much research has focused on what causes these differences. For RNA viruses such as rabies, understanding this rate variability has practical implications, since faster evolution can enable viral emergence in new species or allow a virus to evade its host’s immune defenses. However, nearly all past studies compared viruses of completely different families, and were therefore limited to focusing on viral structural traits. Since few opportunities existed to study the evolution of similar viruses in different host species, the role of the host had been almost completely neglected. Daniel Streicker, a postdoctoral associate in the Odum School of Ecology and the study’s leader, set out to better understand the tempo of evolution of rabies viruses in bats, and specifically what, if any, role the host species played.

To conduct the study, Streicker and his colleagues compiled a database of rabies virus genetic sequences from infected bats in the U.S. and South America, representing 21 different variants of the virus. They also collected information on the biology and ecology of the different bat species that served as viral hosts. They looked at the evolutionary history of the different bat species; their overwintering behavior—whether the bats hibernated, went through periods of torpor, or remained active during the winter; whether the bats were solitary or roosted in colonies; their metabolic rates; and whether the bats engaged in long distance migration. They also classed the bats by climatic region.

Their analysis of this enormous database revealed extreme variability in the rate of evolution in different rabies viruses, comparable to the differences seen between viruses of entirely different families. The analysis also suggested that viral genetic traits were not chiefly responsible for this variation, since rates seemed to shift freely throughout the ancestral history of rabies virus as it jumped into new bat species. “Earlier studies led to the conclusion that viral genomic traits are driving the evolution rate,” Streicker said. “It turns out that’s not the whole story. In this case, host biology plays an important role.”

The trait that best correlated with the rate of viral evolution was not the host’s evolutionary history but its climatic region, which affects the bats’ behavior.

“Species that are widely distributed can have different behaviors in different geographical areas,” Streicker said. “Bats in the tropics are active year-round, so more rabies virus transmission events occur per year. Viruses in hibernating bats, on the other hand, might lose up to six months’ worth of opportunities for transmission.”

Rabies in tropical bats, therefore, goes through more generations per year than in temperate bats, a mechanism that is also hypothesized to accelerate how quickly the molecular clock ticks in free-living tropical plants and animals. The rapid evolution in rabies viruses provided an opportunity to examine one of the mechanisms thought to drive the differences in evolution and species diversity across latitudes from the poles to the tropics. “This is just another example of how the fast pace of evolution in RNA viruses makes them exceptional tools for understanding simultaneously ecological and evolutionary processes,” said Streicker.

Understanding the relationship between geography and rabies viral evolution rates could also shed light on the transmission dynamics of other viruses, such as influenza, that occur across regions.

The team’s findings could eventually help public health officials to better predict when rabies virus transmission could happen in different environments, and as environments change, but Streicker cautioned that more research into the rabies virus genome and the overwintering ecology of bats was needed.

“If viral evolution is faster, it could potentially lead to greater genetic diversity in crucial parts of the viral genome that allow it to shift hosts,” he said. “For rabies, we don’t yet know what those are, so identifying them will be key. Similarly, before understanding whether climate change will speed viral evolution, we need a better idea of how environmental changes will influence host ecology and behavior.”

The paper’s coauthors were Philippe Lemey of the KU Leuven, and Andres Velasco-Villa and Charles E. Rupprecht of the U.S. Centers for Disease Control and Prevention Rabies Program. The research was supported by grants from the University of Georgia, the National Science Foundation, and the European Research Council.


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Rates of viral evolution are linked to host geography in bats
PLoS Pathogens
May 17, 2012