Tiger on the prowl: Invasion history and spatio-temporal genetic structure of the Asian tiger mosquito Aedes albopictus (Skuse 1894) in the Indo-Pacific

Abstract

BackgroundWithin the last century, increases in human movement and globalization of trade have facilitated the establishment of several highly invasive mosquito species in new geographic locations with concurrent major environmental, economic and health consequences. The Asian tiger mosquito, Aedes albopictus, is an extremely invasive and aggressive daytime-biting mosquito that is a major public health threat throughout its expanding range.Methodology/Principal findingsWe used 13 nuclear microsatellite loci (on 911 individuals) and mitochondrial COI sequences to gain a better understanding of the historical and contemporary movements of Ae. albopictus in the Indo-Pacific region and to characterize its population structure. Approximate Bayesian computation (ABC) was employed to test competing historical routes of invasion of Ae. albopictus within the Southeast (SE) Asian/Australasian region. Our ABC results show that Ae. albopictus was most likely introduced to New Guinea via mainland Southeast Asia, before colonizing the Solomon Islands via either Papua New Guinea or SE Asia. The analysis also supported that the recent incursion into northern Australia’s Torres Strait Islands was seeded chiefly from Indonesia. For the first time documented in this invasive species, we provide evidence of a recently colonized population (the Torres Strait Islands) that has undergone rapid temporal changes in its genetic makeup, which could be the result of genetic drift or represent a secondary invasion from an unknown source.Conclusions/SignificanceThere appears to be high spatial genetic structure and high gene flow between some geographically distant populations. The species' genetic structure in the region tends to favour a dispersal pattern driven mostly by human movements. Importantly, this study provides a more widespread sampling distribution of the species’ native range, revealing more spatial population structure than previously shown. Additionally, we present the most probable invasion history of this species in the Australasian region using ABC analysis.

Population genomics of the Asian tiger mosquito, Aedes albopictus: insights into the recent worldwide invasion

“…Our analyses included five Asian samples that cluster into two genetically distinct groups (Figures and ). Interestingly, populations from Singapore and Vietnam show signs of genetic admixture, which is in agreement with mtDNA studies (Maynard et al., ; Zhong et al., ) and suggests ongoing genetic exchange likely with mosquitoes from localities not sampled in this study. A previous study has established that Cluster1 and Cluster2 populations are fully interfertile (O'Donnell & Armbruster, ).…”

“…The discrepancy between this study and that of Manni et al. () could be due to differences in the relative power of the two types of markers used (microstatellite loci vs tens of thousands of SNPs), given that the genetic differentiation between Malaysia–Singapore and USA–Hawaii was also not detected in another microsatellite analysis (Maynard et al., ). Of particular note is the difference in genetic differentiation of the Japanese populations in the two studies.…”

“…Specifically, according to Nazareno, Bemmels, Dick, & Lohmann, (2017) even two samples per population are adequate when >1,500 SNPs are used and accord-ing to the estimations of Patterson, Price, & Reich (2006), if the true Fst between two populations is 0.01 using ~1,000 SNPs, one will need 10 individuals/population. Thus, given the use of >50K SNPs and our Fst estimates (see below in the Results section) and the ones from microsatellites studies (Beebe et al, 2013;Das, Satapathy, Kar, & Hazra, 2014;Kamgang et al, 2011;Manni et al, 2015Manni et al, , 2017Maynard et al, 2017;Minard et al, 2015;Pech-May et al, 2016) Figure 2C and population code are consistent in all the figures of the study. a One individual mosquito excluded from subsequent analyses because of poor sequencing quality.…”

“…Specifically, according to Nazareno, Bemmels, Dick, & Lohmann, () even two samples per population are adequate when >1,500 SNPs are used and according to the estimations of Patterson, Price, & Reich (), if the true Fst between two populations is 0.01 using ~1,000 SNPs, one will need 10 individuals/population. Thus, given the use of >50K SNPs and our Fst estimates (see below in the Results section) and the ones from microsatellites studies (Beebe et al., ; Das, Satapathy, Kar, & Hazra, ; Kamgang et al., ; Manni et al., , ; Maynard et al., ; Minard et al., ; Pech‐May et al., ), sample size used here is well within what is considered adequate. However, to ensure that this is valid in our case organism, we performed some preliminary analyses using two populations (Greece and Italy) of 11 and 16 samples and subsequently, we reduced the number of samples to four for each one and repeated the analyses.…”

“…Many of the phylogeographic and the population genetic studies conducted using nuclear and mitochondrial (mtDNA) markers provided limited resolution because of a combination of factors, including low levels of variation in certain mtDNA markers [but see (Ismail et al, 2015;Porretta, Mastrantonio, Bellini, Somboon, & Urbanelli, 2012;Zhong et al, 2013)], limited population sampling from across the range of the species, and the inability to combine datasets from different studies [for a review on markers used see (Goubert, Minard, Vieira, & Boulesteix, 2016)]. Recent studies utilizing highly variable microsatellite markers represent a significant advance and have begun to illuminate processes of both regional (Maynard et al, 2017;Medley, Jenkins, & Hoffman, 2015) and global range expansion (Manni et al, 2017). Although the previous studies provided important insights into the possible origin of the invasions, their results were sometimes contradictory [e.g., the case of Greece (Kamgang et al, 2011;Manni et al, 2017) or Brazil (Birungi & Munstermann, 2002;Kambhampati, Black, & Rai, 1991)].…”