Aedes aegypti in the Black Sea: recent introduction or ancient remnant?

Abstract

BackgroundThe yellow fever mosquito Aedes aegypti transmits viral diseases that have plagued humans for centuries. Its ancestral home are forests of Africa and ~400–600 years ago it invaded the New World and later Europe and Asia, causing some of the largest epidemics in human history. The species was rarely detected in countries surrounding the Mediterranean Sea after the 1950s, but during the last 16 years it re-appeared in Madeira, Russia and in the eastern coast of the Black Sea. We genotyped Ae. aegypti populations from the Black Sea region to investigate whether this is a recent invasion (and if so, where it came from) or a remnant of pre-eradication populations that extended across the Mediterranean. We also use the Black Sea populations together with a world reference panel of populations to shed more light into the phylogeographical history of this species.ResultsMicrosatellites and ~19,000 genome-wide single nucleotide polymorphisms (SNPs) support the monophyletic origin of all populations outside Africa, with the New World as the site of first colonization. Considering the phylogenetic relationships, the Black Sea populations are basal to all Asian populations sampled. Bayesian analyses combined with multivariate analyses on both types of markers suggest that the Black Sea population is a remnant of an older population. Approximate Bayesian Computation Analysis indicates with equal probability, that the origin of Black Sea populations was Asia or New World and assignment tests favor the New World.ConclusionsOur results confirmed that Ae. aegypti left Africa and arrived in New World ~500 years ago. The lineage that returned to the Old World and gave rise to present day Asia and the Black Sea populations split from the New World approximately 100–150 years ago. Globally, the Black Sea population is genetically closer to Asia, but still highly differentiated from both New World and Asian populations. This evidence, combined with bottleneck signatures and divergence time estimates, support the hypothesis of present day Black Sea populations being remnants of older populations, likely the now extinct Mediterranean populations that, consistent with the historic epidemiological record, likely represent the original return of Ae. aegypti to the Old World.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2933-2) contains supplementary material, which is available to authorized users.

Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa

“…() favored the New World coming from Asia, although the statistical support for this biogeographic scenario was not strong. Our data here (Figure ) and elsewhere (Brown et al., ; Gloria‐Soria et al., ; Kotsakiozi et al., ) support with strong statistical power that Asia was derived from the New World.…”

“…We sampled 20 populations of Aedes aegypti originating from continental Africa and nearby Reunion Island (Figure , Table ) covering a large part of the Aaf distribution. We also used 10 previously studied populations (Gloria‐Soria et al., ; Kotsakiozi et al., ) of Aaa originating from the New World and Asia (Table ). Aedes mascarensis from the island of Mauritius was used as an outgroup; this species is very closely related to Ae.…”

“…We sampled 20 populations of Aedes aegypti originating from continental Africa and nearby Reunion Island ( Figure 1, Table 1) covering a large part of the Aaf distribution. We also used 10 previously studied populations Kotsakiozi et al, 2018) of Aaa originating from the New World and Asia (Table 1).…”

“…mascarensis was used as an outgroup, and Aaa samples from New World and Asia were used to test the distinctiveness of Aaf and Aaa lineages. Bootstraps are presented on the nodes; values <70 are not shown Using genetic data, the time of origin of Aaa in the New World has been estimated to be ~400-500 years ago (Crawford et al, 2017;Gloria-Soria et al, 2016;Kotsakiozi et al, 2018). Yellow fever was first reported in the New World in 1648 (McNeill, 1976) not long after the introduction of Ae.…”

“…While populations outside Africa (largely conforming to Aaa) have been well-studied and strong genetic structure among and within continents have been documented [e.g., (Bosio et al, 2005;Bracco, Capurro, Lourenço-de-Oliveira, & Sallum, 2007;Brown et al, 2011Brown et al, , 2014Gloria-Soria et al, 2016;Gonçalves da Silva et al, 2012;Kotsakiozi, Gloria-Soria, Schaffner, Robert, & Powell, 2018;Kotsakiozi, Gloria-Soria et al, 2017;Mousson, Dauga, Garrigues, & Schaffner, 2005;Pless et al, 2017;Rašić et al, 2015;Scarpassa, Cardoza, & Cardoso, 2008)], the ancestral populations in Africa have been understudied. Even Ae.…”