RESEARCH ARTICLE Zika virus outbreak in the Pacific: Vector competence of regional vectors Elodie Calvez1, Laurence Mousson2, Marie Vazeille2, Olivia O'Connor1, Van-Mai Cao- Lormeau3, FrancËoise Mathieu-Daude 4, Nicolas Pocquet5, Anna-Bella Failloux2³, Myrielle Dupont-Rouzeyrol1³* 1 Institut Pasteur de Nouvelle-CaleÂdonie, URE-Dengue et autres Arboviroses, NoumeÂa, New Caledonia, 2 Institut Pasteur, Arboviruses and Insect Vectors Laboratory, Paris, France, 3 Unit of Emerging Infectious Diseases, Institut Louis Malarde, French Polynesia & Aix Marseille Univ, IRD, AP-HM, SSA, VITROME, IHU- MeÂditeÂrraneÂe Infection, Marseille, France, 4 Institut de Recherche pour le DeÂveloppement, UMR MIVEGEC IRD, CNRS, UM, Montpellier, France, 5 Institut Pasteur de Nouvelle-CaleÂdonie, URE-Entomologie MeÂdicale, a1111111111 NoumeÂa, New Caledonia a1111111111 a1111111111 ³ These authors are joint senior authors on this work. a1111111111 * [email protected] a1111111111 Abstract OPEN ACCESS Background Citation: Calvez E, Mousson L, Vazeille M, In 2013, Zika virus (ZIKV) emerged in French Polynesia and spread through the Pacific O'Connor O, Cao-Lormeau V-M, Mathieu-Daude F, region between 2013 and 2017. Several potential Aedes mosquitoes may have contributed et al. (2018) Zika virus outbreak in the Pacific: Vector competence of regional vectors. PLoS Negl to the ZIKV transmission including Aedes aegypti, the main arbovirus vector in the region, Trop Dis 12(7): e0006637. https://doi.org/10.1371/ and Aedes polynesiensis, vector of lymphatic filariasis and secondary vector of dengue journal.pntd.0006637 virus. The aim of this study was to analyze the ability of these two Pacific vectors to transmit Editor: Benjamin Althouse, Institute for Disease ZIKV at a regional scale, through the evaluation and comparison of the vector competence Modeling, UNITED STATES of wild Ae. aegypti and Ae. polynesiensis populations from different Pacific islands for a Received: February 22, 2018 ZIKV strain which circulated in this region during the 2013±2017 outbreak. Accepted: June 25, 2018 Methodology/principal findings Published: July 17, 2018 Field Ae. aegypti (three populations) and Ae. polynesiensis (two populations) from the Pacific Copyright: © 2018 Calvez et al. This is an open 7 access article distributed under the terms of the region were collected for this study. Female mosquitoes were orally exposed to ZIKV (10 Creative Commons Attribution License, which TCID50/mL) isolated in the region in 2014. At 6, 9, 14 and 21 days post-infection, mosquito permits unrestricted use, distribution, and bodies (thorax and abdomen), heads and saliva were analyzed to measure infection, dissem- reproduction in any medium, provided the original ination, transmission rates and transmission efficiency, respectively. According to our results, author and source are credited. ZIKV infection rates were heterogeneous between the Ae. aegypti populations, but the dis- Data Availability Statement: All relevant data are semination rates were moderate and more homogenous between these populations. For Ae. within the paper and its Supporting Information files. polynesiensis, infection rates were less heterogeneous between the two populations tested. The transmission rate and efficiency results revealed a low vector competence for ZIKV of Funding: This work was supported by the Actions ConcerteÂes Inter Pasteuriennes (ZikAe Project, the different Aedes vector populations under study. ACIP A-15-2014). This work was partly funded by the European Union's Horizon 2020 Research and Conclusion/significance Innovation Programme under ZIKAlliance Grant Agreement No. 734548 and by the Ministère des Our results indicated a low ZIKV transmission by Ae. aegypti and Ae. polynesiensis tested Outre-mer (SEOM). The funders had no role in from the Pacific region. These results were unexpected and suggest the importance of other PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0006637 July 17, 2018 1 / 12 Zika virus and Aedes mosquitoes from the Pacific region study design, data collection and analysis, decision factors especially the vector density, the mosquito lifespan or the large immunologically to publish, or preparation of the manuscript. naive fraction of the population that may have contributed to the rapid spread of the ZIKV in Competing interests: The authors have declared the Pacific region during the 2013±2017 outbreak. that no competing interests exist. Author summary Zika virus (ZIKV) was isolated for the first time in Uganda in 1947. The virus was sporadi- cally detected in Africa and Asia during few decades. The first human outbreak was declared in Yap Island in Micronesia in 2007. The virus reemerged in 2013 in French Polynesia and circulated throughout the Pacific region and in Americas between 2013 and 2017. ZIKV is transmitted to human by the bite of an infected mosquito. Aedes mosqui- toes were particularly incriminated in the ZIKV outbreak. In this study, we showed for the first time the results of vector competence study of wild Aedes aegypti and Aedes poly- nesiensis from different islands of the Pacific region. Our results demonstrated an unex- pected homogenous and low ZIKV vector competence for the different populations of these two vectors. These findings seemed to indicate that other factors have contributed to the rapid spread of ZIKV in the Pacific region. Introduction Zika fever is an emerging vector borne disease caused by a single stranded RNA virus, Zika virus (ZIKV) belonging to the genus Flavivirus [1]. ZIKV is transmitted to humans by the bite of infected vectors mainly Aedes mosquitoes [2±4]. Since its first isolation in Uganda in 1947, ZIKV has been detected occasionally in Africa and Asia [5]. The first human outbreak was declared in Yap state in Federated States of Micronesia in 2007 [4]. ZIKV reemerged in the Pacific region in 2013 in French Polynesia and then spread across the region and to the Ameri- cas between 2014 and 2016 [5±9]. This recent outbreak was associated with neurological disor- ders as Guillain-Barre syndrome [10±12], myasthenia gravis [13] and microcephaly [14, 15] were reported in the Pacific region and in South and Central America including the Caribbean (http://www.paho.org). Phylogenetic studies indicated that ZIKV is divided into two lineages: African and Asian with less than 12% of genetic divergence [16, 17]. The 2013±2016 outbreak was due to the emergence of ZIKV belonging to Asian lineage, and genetic analysis revealed divergence between the Pacific and the American clades [18, 19]. During the 2013 French Polynesian ZIKV outbreak, more than 8,700 suspected cases and 30,000 medical consultations were reported by the sentinel surveillance network [10]. A recent seroprevalence study estimated that more than half of the population was infected by ZIKV dur- ing the outbreak in this territory [20]. From French Polynesia, the disease spread to New Cale- donia in 2013 [7, 21] affecting the whole territory. Based on the number and proportion of confirmed cases and the proportion of ZIKV infections among arboviral syndromes recorded in the population, New Caledonia Health Authorities estimated the number of cases at about 11,000 [11]. From 2014 to 2017, ZIKV was detected in the Cook Islands, Vanuatu, Fiji, Samoa, Salomon Islands, Tonga and American Samoan (http://www.spc.int/phd/epidemics/)[14, 22]. In the Pacific landscape, different mosquito species are present and some of them are known as potential arbovirus vectors, especially mosquitoes from Aedes genus. Ae. aegypti is present in most Pacific islands with few exceptions [23]. The presence of Ae. albopictus is confirmed in 5 out of 17 countries and territories of this region and its expansion through the Western Pacific PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0006637 July 17, 2018 2 / 12 Zika virus and Aedes mosquitoes from the Pacific region islands is observed right up to Fiji and Tonga islands [24, 25]. Ae. polynesiensis distribution is reported in the Eastern part of the Pacific, from French Polynesia to Fiji [22]. In addition, the presence of other vectors is recorded in some local parts of the Pacific region as Aedes hensilli, Aedes scutellaris and other Aedes species belonging to the scutellaris group ([26±28]. Previous studies evaluated the vector competence of Aedes vectors for ZIKV belonging to both lineages. Mosquitoes from Africa [29], Asia [30, 31] and America [32, 33] were infected by ZIKV strains belonging to the African lineage and showed various results. The vector com- petence for ZIKV belonging to the Asian lineage was also evaluated with vectors from America [2, 34] Australia [35] and Europe [36]. However, the ability of the vectors from the Pacific to transmit ZIKV has been poorly studied. Ae. hensilli from Yap island, appeared to be able to dis- seminate African ZIKV strain but the transmission has not been evaluated. However this mos- quito was the most collected species in Yap island, Federated States of Micronesia, during the ZIKV outbreak in 2007 (41%) supporting its possible role as a vector during the outbreak [27]. Laboratory strains of Ae. aegypti and Ae. polynesiensis from French Polynesia were shown to be able to get infected and disseminate an Asian/Pacific ZIKV strain isolated in French Polyne- sia in 2013. Furthermore, infectious ZIKV particles have been found in saliva of Ae. aegypti from French Polynesia as soon as 6 days post-infection [37]. The Pacific landscape promotes specific environmental