Genetic evidence for the origin of Aedes aegypti, the yellow fever mosquito, in the southwestern Indian Ocean

Abstract

Aedes aegypti is among the best-studied mosquitoes due to its critical role as a vector of human pathogens and ease of laboratory rearing. Until now, this species was thought to have originated in continental Africa, and subsequently colonized much of the world following the establishment of global trade routes. However, populations of this mosquito on the islands in the southwestern Indian Ocean (SWIO), where the species occurs with its nearest relatives referred to as the Aegypti Group, have received little study. We re-evaluated the evolutionary history of Ae. aegypti and these relatives, using three data sets: nucleotide sequence data, 18,489 SNPs and 12 microsatellites. We found that: (a) the Aegypti Group diverged 16 MYA (95% HPD: 7-28 MYA) from its nearest African/Asian ancestor; (b) SWIO populations of Ae. aegypti are basal to continental African populations; (c) after diverging 7 MYA (95% HPD: 4-15 MYA) from its nearest formally described relative (Ae. mascarensis), Ae. aegypti moved to continental Africa less than 85,000 years ago, where it recently (<1,000 years ago) split into two recognized subspecies Ae. aegypti formosus and a human commensal, Ae. aegypti aegypti; (d) the Madagascar samples form a clade more distant from all other Ae. aegypti than the named species Ae. mascarensis, implying that Madagascar may harbour a new cryptic species; and (e) there is evidence of introgression between Ae. mascarensis and Ae. aegypti on Réunion, and between the two subspecies elsewhere in the SWIO, a likely consequence of recent introductions of domestic Ae. aegypti aegypti from Asia.

Keywords: insects; invasive species; population genetics—empirical; systematics.

FIGURE 1

Map of the southwestern Indian Ocean, east of Africa. Estimates of island ages are from Ashwal et al. (2017), Warren et al. (2003) and Michon (2016). While Ae. aegypti is found on Madagascar and all islands highlighted, Ae. mascarensis is endemic to Mauritius, and Ae pia is endemic to Mayotte [Colour figure can be viewed at wileyonlinelibrary.com]

FIGURE 2

Divergence times in the Aegypti Group correlate with island formations for Aedes pia and Aedes mascarensis. Divergence times shown here based on the relaxed clock analysis in BEAST2 for members of the Stegomyia subgenus Aedes. Relationships among clades in the subgenus Stegomyia show here are concordant with the maximum‐likelihood analyses performed, as well (see Figure S1). The first support value indicates is the ultrafast bootstrap support value from IQ‐Tree, while the second is the posterior probability from BEAST2 [Colour figure can be viewed at wileyonlinelibrary.com]

FIGURE 3

Genetic diversity in the Aegypti Group. (a) A PCA demonstrating that island populations cluster separately from the recognized subspecies Aedes aegypti aegypti (Aaa) and Aedes aegypti formosus (Aaf). (b) A visual depiction of TreeMix results demonstrating the most likely admixture scenarios involving the three admixed populations of Mayotte, Réunion and Mombasa in Kenya. In all three cases, the most likely scenario had one parental "donor" from Jeddah, although other Asian populations are possible, as well; see Sections 3 and 4 for additional details

FIGURE 4

The maximum‐likelihood phylogeny estimated from Aegypti Group SNP data demonstrates the deep divergence of Aedes aegypti from Madagascar from populations of Aedes aegypti s.s. Narrow coloured vertical bars reflect species or population of origin. Black and grey bars reflect populations of Aedes aegypti s.s. assigned to one of the two subspecies Aedes aegypti formosus (Aaf) or Aedes aegypti aegypti (Aaa). The phylogeny was estimated in IQ‐Tree and was rooted on the branch leading to Aedes pia. Support values are ultrafast bootstraps estimated in IQ‐Tree, and branches with support values below 90 have been collapsed. Scale is in substitutions per site