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. 2022 Jul 25;12(7):e9138.
doi: 10.1002/ece3.9138. eCollection 2022 Jul.

Multiple introductions and overwintering shape the progressive invasion of Aedes albopictus beyond the Alps

Affiliations

Multiple introductions and overwintering shape the progressive invasion of Aedes albopictus beyond the Alps

Laura Vavassori et al. Ecol Evol. .

Abstract

Aedes albopictus originates from Southeast Asia and is considered one of the most invasive species globally. This mosquito is a nuisance and a disease vector of significant public health relevance. In Europe, Ae. albopictus is firmly established and widespread south of the Alps, a mountain range that forms a formidable biogeographic barrier to many organisms. Recent reports of Ae. albopictus north of the Alps raise questions of (1) the origins of its recent invasion, and (2) if this mosquito has established overwintering populations north of the Alps. To answer these questions, we analyzed population genomic data from >4000 genome-wide SNPs obtained through double-digest restriction site-associated DNA sequencing. We collected SNP data from specimens from six sites in Switzerland, north and south of the Alps, and analyzed them together with specimens from other 33 European sites, five from the Americas, and five from its Asian native range. At a global level, we detected four genetic clusters with specimens from Indonesia, Brazil, and Japan as the most differentiated, whereas specimens from Europe, Hong Kong, and USA largely overlapped. Across the Alps, we detected a weak genetic structure and high levels of genetic admixture, supporting a scenario of rapid and human-aided dispersal along transportation routes. While the genetic pattern suggests frequent re-introductions into Switzerland from Italian sources, the recovery of a pair of full siblings in two consecutive years in Strasbourg, France, suggests the presence of an overwintering population north of the Alps. The suggestion of overwintering populations of Ae. albopictus north of the Alps and the expansion patterns identified points to an increased risk of further northward expansion and the need for increased surveillance of mosquito populations in Northern Europe.

Keywords: Asian tiger mosquito; fine‐scale population genomics; human‐assisted dispersal; overwintering; recent invasion; skip oviposition.

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Conflict of interest statement

The authors declare no competing interests.

Figures

FIGURE 1
FIGURE 1
Aedes albopictus sampling sites. The pie charts represent collection sites, where the size of each pie represents how many individuals were collected in each location. The panels represent the sampling sites at the (a) global, (b) Europe, and (c) Swiss levels.
FIGURE 2
FIGURE 2
Genetically distinct clusters of Ae. albopictus sampled populations. Four genetic clusters may be observed in the global dataset (1.native_invasive_cleaned) based on the PCA and DAPC analysis. (a) PCA with the percent variation explained by the first two principal components (b) Scatterplot showing the results from the DAPC (K = 4).
FIGURE 3
FIGURE 3
Aedes albopictus ADMIXTURE barplot for all mosquito populations based on the results from the dataset 1.native_invasive_cleaned. Each bar represents one individual, while white vertical lines indicate separate countries. Country codes: AL: Albania, AU: Austria, BR: Brazil, CH: Switzerland, HK: Hong Kong, DE: Germany, FR: France, GR: Greece, ID: Indonesia, FL: Liechtenstein, IT: Italy, JP: Japan and US: USA.
FIGURE 4
FIGURE 4
Output of the fineRADstructure analysis of the 1.native_invasive dataset. The heat map indicates pairwise co‐ancestry between individuals, with black, blue, and purple representing the highest levels, red and orange indicating intermediate levels, and yellow representing the lowest levels of shared co‐ancestry. The tree on top of the heat map shows the inferred relationships between the specimens analyzed, with each tip corresponding to an individual. On the Y‐axis, country of origin with their sample collection site ID is reported if they create distinct clusters, otherwise are included in the Europe (rest) cluster. On the X‐axis, sample codes are encoded with their laboratory ID (see Appendix S1: Table S1). Siblings are depicted in black and blue colors.
FIGURE 5
FIGURE 5
ADMIXTURE barplot obtained for the 2.europe_cleaned dataset for K = 2–3. Individuals represented by vertical bars along the plot grouped by country and collection site. The Y‐axis represents the probability of an individual to be assigned to a genetic cluster. Each cluster is given in a different color. Multi‐colored bars indicate admixed genetic ancestry in the respective individual. The white vertical lines indicate country limits. Country codes: AL: Albania, CH: Switzerland, DE: Germany, FR: France, GR: Greece, IT: Italy.
FIGURE 6
FIGURE 6
Genetic structure and differentiation of Ae. albopictus specimens collected in Europe. (a) Scatterplot showing the results of the DAPC (K = 3) on the 2.europe_cleaned dataset. Cluster 1‐purple includes mosquitoes collected in Albania with some specimens collected in Greece; cluster 2‐green includes mosquitoes collected in Northern Italy (with the exception of two specimens which clustered with cluster 3 (orange), mosquitoes collected in southern and northern Switzerland and one specimen from Germany. Cluster 3‐orange includes specimens collected in Italy‐Center‐South, Italy‐Sicily, Switzerland, and France. (b) Neighbor‐net network of D ps relative genetic distances among the specimens from Italy. The map shows the locations of the sampling in the region of Italy‐Center‐South and Italy‐Sicily. Specimens collected in Northern Italy are depicted with a green square (cluster 2 ‐ green) and the one collected in Central and Southern Italy with orange circles (cluster 3 ‐ orange). Specimens from the Italian island Sicily are not reported here. For the sample abbreviations, see Appendix S1, Table S1 Laboratory ID.
FIGURE 7
FIGURE 7
Genomic diversity of Ae. albopictus collected in Italy and in Switzerland. (a) Individual observed heterozygosity (H_obs) estimated with VCFtools on the 2.europe_cleaned dataset. The individuals were grouped by geographical regions, including three regions in Italy and two regions in Switzerland, and difference in their mean heterozygosity (H O) was tested with the non‐parametric Kruskal–Wallis (KW) test. (b) H_obs in the samples collected in Switzerland from the same sites in 2017 and 2018. (c) F IS calculated between samples collected in the three sites in Switzerland in 2017 and in 2018. (d) Inbreeding coefficient F IS between specimens collected from the same sites in Switzerland in 2017 and 2018.
FIGURE 8
FIGURE 8
Isolation by distance (IBD) analysis using the 2.europe_cleaned dataset represented as scatterplots. (a) Correlation of genetic distances as proportion of shared alleles (D ps) and geographic distances on logarithmic scale for samples from Italy (excluding samples from Sicily). The correlation was assessed using a Mantel test, R = −0.16, p‐value = .974 based on 999 replicates. (b) Correlation between D ps genetic distances and logarithmic geographic distances for samples from Northern Italy and southern Switzerland. The correlation was assessed using a Mantel test based on 999 replicates, Mantel R = −0.17, p‐value = .988.
FIGURE 9
FIGURE 9
Genetic assignment tests. (a) Assignment accuracy estimated by Monte Carlo cross‐validation based on the 2. europe_cleaned dataset. Assigned source populations were France (pop_fr) and Northern Italy (pop_itnd). Red horizontal lines indicate 0.33 null assignment rate, where the assignment accuracy is zero. (b) Membership probability of the individuals collected in Switzerland, organized from north to south. Individuals are sorted based on the probability of assignment to their original populations.

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