Understanding the evolution and spread of chikungunya virus in the Americas using complete genome sequences

Abstract

Local transmission of chikungunya virus (CHIKV) was first detected in the Americas in December 2013, after which it spread rapidly throughout the Caribbean islands and American mainland, causing a major chikungunya fever epidemic. Previous phylogenetic analysis of CHIKV from a limited number of countries in the Americas suggests that an Asian genotype strain was responsible, except in Brazil where both Asian and East/Central/South African (ECSA) lineage strains were detected. In this study, we sequenced thirty-three complete CHIKV genomes from viruses isolated in 2014 from fourteen Caribbean islands, the Bahamas and two mainland countries in the Americas. Phylogenetic analyses confirmed that they all belonged to the Asian genotype and clustered together with other Caribbean and mainland sequences isolated during the American outbreak, forming an ‘Asian/American’ lineage defined by two amino acid substitutions, E2 V368A and 6K L20M, and divided into two well-supported clades. This lineage is estimated to be evolving at a mean rate of 5 × 10−4 substitutions per site per year (95% higher probability density, 2.9–7.9 × 10−4) and to have arisen from an ancestor introduced to the Caribbean (most likely from Oceania) in about March 2013, 9 months prior to the first report of CHIKV in the Americas. Estimation of evolutionary rates for individual gene regions and selection analyses indicate that (in contrast to the Indian Ocean Lineage that emerged from the ECSA genotype followed by adaptive evolution and with a significantly higher substitution rate) the evolutionary dynamics of the Asian/American lineage are very similar to the rest of the Asian genotype and natural selection does not appear to have played a major role in its emergence. However, several codon sites with evidence of positive selection were identified within the non-structural regions of Asian genotype sequences outside of the Asian/American lineage.

Differential Effects of Temperature and Mosquito Genetics Determine Transmissibility of Arboviruses by Aedes aegypti in Argentina

“…This population-specific competence is similar to what has been reported in other studies, 16,20 yet our results suggest that CHIKV competence is more dependent on mosquito population than DENV competence, perhaps reflecting the shorter evolutionary history of this virus in the region. 36,37 Whereas this suggests that further adaptive evolution of CHIKV in the region could enhance transmission, 38 an important caveat of these studies is that a single CHIKV isolate was used and other viral genotypes could be inherently more transmissible. 39 Although previous findings of increased temperatures resulting in decreased extrinsic incubation and increased competence are generally supported by our data, 6,7,9 results also demonstrate that fluctuations in temperature will have both virus species-and population-specific effects on competence.…”

Chikungunya virus outbreak in the Amazon region: replacement of the Asian genotype by an ECSA lineage

“…Lineage-specific clinical presentations have been recently highlighted by a recent index cluster study which showed that 82% of CHIKV infections caused by the ECSA lineage are symptomatic, in comparison to only 52% of symptomatic infections caused by the Asian genotype [54]. While the Asian lineage seems to have circulated cryptically for 9 months before its first detection in the Caribbean [3], the faster detection of the ECSA lineage in Brazil could at least in part be a consequence of a higher rate of symptomatic to asymptomatic infections of the ECSA lineage circulating in Brazil. The time lag between the phylogenetic estimate of the date of introduction of a virus lineage and the date of the first confirmed case in a given region, enables us to identify surveillance gaps between the arrival and discovery of a virus in that region [69].…”

Epidemiological Aspects and Modern Evolution of Globally Spreading Arboviruses

“…Доказано, в частности, что мутации E1-K211E и E2-V264A повышают инфекционность вируса в отношении Ae. aegypti [30,36,40].…”

“…Высказывается мнение, что это способствовало дальнейшему расширению распространения восточно-центрально-южноафриканской линии вируса и привело к возможности реализации непродолжительной по времени локальной передачи CHIKV на новых для него «северных» территориях, в частности, в регионах Европейского Средиземноморья (побережье Италии, Франции), где плотность популяций Ae. albopictus высока [36].…”

“…aegypti. К другим вариантам адаптивных мутаций в структуре гена белка оболочки относят замены E1-M407L, E1-T98A, E2-A103T, обнаруженные в бразильских изолятах CHIKV [30,36,40,47].…”