Natural colonization and adaptation of a mosquito species in Galapagos and its implications for disease threats to endemic wildlife

Abstract

Emerging infectious diseases of wildlife have been recognized as a major threat to global biodiversity. Endemic species on isolated oceanic islands, such as the Galápagos, are particularly at risk in the face of introduced pathogens and disease vectors. The black salt-marsh mosquito (Aedes taeniorhynchus) is the only mosquito widely distributed across the Galápagos Archipelago. Here we show that this mosquito naturally colonized the Galápagos before the arrival of man, and since then it has evolved to represent a distinct evolutionary unit and has adapted to habitats unusual for its coastal progenitor. We also present evidence that A. taeniorhynchus feeds on reptiles in Galápagos in addition to previously reported mammal and bird hosts, highlighting the important role this mosquito might play as a bridge-vector in the transmission and spread of extant and newly introduced diseases in the Galápagos Islands. These findings are particularly pertinent for West Nile virus, which can cause significant morbidity and mortality in mammals (including humans), birds, and reptiles, and which recently has spread from an introductory focus in New York to much of the North and South American mainland and could soon reach the Galápagos Islands. Unlike Hawaii, there are likely to be no highland refugia free from invading mosquito-borne diseases in Galápagos, suggesting bleak outcomes to possible future pathogen introduction events.

Fig. 1.

Map of the sites where Aedes taeniorhynchus specimens were collected on the American continents and on the Galápagos Islands. Numbers between brackets are the number of specimens collected in each site used for the mtDNA and microsatellite studies, respectively. Sites where bloodmeals from bloodfed mosquitoes were analyzed are underlined.

Fig. 2.

Unrooted Bayesian tree based on combined COII and ND5 mtDNA gene datasets (A) and unrooted distance tree based on proportion of shared alleles (B), showing the relationships between A. taeniorhynchus populations. Haplotype and population name codes refer to names given in Fig. 1 and Table S1. Numbers beside branches indicate supports for the nodes of the trees from posterior probability/bootstrap values (> 50%) obtained with Bayesian inference and maximum likelihood methods, respectively (A), and bootstrap values (>50%) from shared allele and Cavalli-Sforza distance calculations, respectively (B). The Galápagos cluster is highlighted by a gray circle. Highland populations are surrounded by a rectangle in B.

Fig. 3.

Results of Bayesian individual clustering for the Galápagos microsatellite dataset (A), and of Bayesian population clustering for the Galápagos dataset (B). In both A and B, individuals are grouped by sampling location (or geographical entities) within each island. Abbreviations shown between the 2 panels are code names of sampling locations referring to codes given in Fig. 1. (A) Each individual is represented by a vertical bar partitioned into colored segments according to the probability of belonging to one of the K-color-coded genetic clusters, K being defined as the number of clusters that best fit with our data (here K = 6, identified by the 6 colors in the graph). (B) In the population clustering, the sampling locations/geographical entities are grouped by color to indicate which groups are likely to represent distinct populations. Highland populations are indicated with labels highlighted in gray.