Tracing the tiger: population genetics provides valuable insights into the Aedes (Stegomyia) albopictus invasion of the Australasian Region

Abstract

Background: The range of the Asian tiger mosquito Aedes albopictus is expanding globally, raising the threat of emerging and re-emerging arbovirus transmission risks including dengue and chikungunya. Its detection in Papua New Guinea's (PNG) southern Fly River coastal region in 1988 and 1992 placed it 150 km from mainland Australia. However, it was not until 12 years later that it appeared on the Torres Strait Islands. We hypothesized that the extant PNG population expanded into the Torres Straits as an indirect effect of drought-proofing the southern Fly River coastal villages in response to El Nino-driven climate variability in the region (via the rollout of rainwater tanks and water storage containers).

Methodology/principal findings: Examination of the mosquito's mitochondrial DNA cytochrome oxidase I (COI) sequences and 13 novel nuclear microsatellites revealed evidence of substantial intermixing between PNG's southern Fly region and Torres Strait Island populations essentially compromising any island eradication attempts due to potential of reintroduction. However, two genetically distinct populations were identified in this region comprising the historically extant PNG populations and the exotic introduced population. Both COI sequence data and microsatellites showed the introduced population to have genetic affinities to populations from Timor Leste and Jakarta in the Indonesian region.

Conclusions/significance: The Ae. albopictus invasion into the Australian region was not a range expansion out of PNG as suspected, but founded by other, genetically distinct population(s), with strong genetic affinities to populations sampled from the Indonesian region. We now suspect that the introduction of Ae. albopictus into the Australian region was driven by widespread illegal fishing activity originating from the Indonesian region during this period. Human sea traffic is apparently shuttling this mosquito between islands in the Torres Strait and the southern PNG mainland and this extensive movement may well compromise Ae. albopictus eradication attempts in this region.

Figure 1. Map of the region under study and mosquito collection sites (Panel A).

An expanded view of the region inhabited by the recently introduced Ae. albopictus population (red box) with collection sites indicated in Panel B. Colored triangles correspond to sample locations.

Figure 2. Mitochondrial COI haplotype network showing the 16 haplotypes identified throughout PNG and the Australian region.

Haplotypes are colored by region and the size of their circle is proportional to number of individuals showing that haplotype sequence with each connection a single mutational step.

Figure 3. Panel A: Microsatellite Bayesian Structure Plot for Ae. albopictus.

Thirteen microsatellite markers were run on 199 Ae. albopictus individuals assuming five populations (K = 5). Each bar represents an individual with the color of the bar the probability of the individual belonging to a genetic population or cluster. Panel B: The structure plot results (K = 5) integrated into a map of the region with the locations of each population shown.

Figure 4. Factorial Correspondence Analysis (FCA) of 199 Ae. albopictus individuals.

Each point represents one individual assessed for 13 microsatellites with their relative proximity to each other on the graph representing genetic relatedness. Panels A and B represent two perspectives of the graph.