The worldwide spread of Aedes albopictus: New insights from mitogenomes

Abstract

The tiger mosquito (Aedes albopictus) is one of the most invasive species in the world and a competent vector for numerous arboviruses, thus the study and monitoring of its fast worldwide spread is crucial for global public health. The small extra-nuclear and maternally-inherited mitochondrial DNA represents a key tool for reconstructing phylogenetic and phylogeographic relationships within a species, especially when analyzed at the mitogenome level. Here the mitogenome variation of 76 tiger mosquitoes, 37 of which new and collected from both wild adventive populations and laboratory strains, was investigated. This analysis significantly improved the global mtDNA phylogeny of Ae. albopictus, uncovering new branches and sub-branches within haplogroup A1, the one involved in its recent worldwide spread. Our phylogeographic approach shows that the current distribution of tiger mosquito mitogenome variation has been strongly affected by clonal and sub-clonal founder events, sometimes involving wide geographic areas, even across continents, thus shedding light on the Asian sources of worldwide adventive populations. In particular, different starting points for the two major clades within A1 are suggested, with A1a spreading mainly along temperate areas from Japanese and Chinese sources, and A1b arising and mainly diffusing in tropical areas from a South Asian source.

Keywords: Aedes albopictus spread; MtDNA variation; haplogroups; mitogenome; phylogeny; sources of adventive populations.

FIGURE 1

Phylogeny of Ae. albopictus mitogenomes. The tree encompasses 37 novel (circles marked by a thicker line) and 39 previously published sequences (24 from Battaglia et al., 2016, 1 from Zhang et al., 2015, 14 from Zé-Zé et al., 2020). The asterisk (*) refers to the 363 mutations (347 and 16 in the coding- and control-regions, respectively), listed in Supplementary Figure S1 (Battaglia et al., 2016), separating mitogenome #76 from the A1’2 node. For the phylogeny construction, the entire coding-region variation of all mitogenomes was included as well as some control-region mutations (from np 14897 to np 15350 and from np 16831 to np17150). The mitogenome from a mosquito of the Italian Rimini strain (#1, marked by the arrow) was employed to number the mutations shown on the branches. Mutations are transitions, unless a base is appended to indicate a transversion (to A, G, C, or T), or a suffix for indels (1, d). Heteroplasmic positions are indicated using the IUPAC nucleotide code. Recurrent mutations within the phylogeny are underlined (and in italics if present in mitogenome #76) and back mutations are marked with the suffix @. The numerous mutations shared only by the published mitogenomes #42 and #76 are marked with the suffix §. Sequences from Portugal (Zé-Zé et al., 2020) are from np 283 to np 14702; mutations out of this range were inferred according to their position in the tree. Colours illustrate geographic origins. Length variation (insertions/deletions) in polynucleotide stretches beginning at nps 3808, 8134, and 17140 were not considered. Haplogroups in blue are new relative to Battaglia et al., 2016. Non-synonymous mutations are indicated with squares, with colours matching the protein-coding gene complexes (top left in the figure); mutations in 12S and 16S rRNA genes are shown too, with blue and red diamonds. The MP tree is shown in the top inset; branch lengths are not proportional to molecular divergence.

FIGURE 2

Possible worldwide diffusion routes of Ae. albopictus. Arrows indicate postulated diffusion routes from the native home-range (South-East Asia) and subsequent dispersals of major clades and subclades within haplogroup A1. The original world map is from the website (http://www.freeworldmaps.net).