Population genomics of two invasive mosquitoes (Aedes aegyptiandAedes albopictus) from the Indo-Pacific

Abstract

The arbovirus vectors Aedes aegypti (yellow fever mosquito) and Ae. albopictus (Asian tiger mosquito) are both common throughout the Indo-Pacific region, where 70% of global dengue transmission occurs. For Ae. aegypti all Indo-Pacific populations are invasive, having spread from an initial native range of Africa, while for Ae. albopictus the Indo-Pacific includes invasive populations and those from the native range: putatively, India to Japan to Southeast Asia. This study analyses the population genomics of 480 of these mosquitoes sampled from 27 locations in the Indo-Pacific. We compared patterns of genetic differentiation to investigate pathways of invasion and ongoing gene flow in both species, and to infer potential native-range boundaries and cryptic subspecies in Ae. albopictus. We also tested landscape genomic hypotheses that genetic differentiation would increase with geographical distance and be lower between locations with high connectivity to human transportation routes, the primary means of dispersal at these scales. We found that genetic distances were generally higher in Ae. aegypti, with Pacific populations the most highly differentiated. The most differentiated Ae. albopictus populations were in Vanuatu, Indonesia and Sri Lanka; the latter two may represent ancestral native-range populations or cryptic subspecies, respectively. Genetic distances in Ae. aegypti increased with geographical distance, while in Ae. albopictus they decreased with higher connectivity to human transportation routes. Contrary to in Ae. aegypti, we found evidence of long-distance Ae. albopictus colonisation events, including of Mauritius from East Asia and of Fiji from Southeast Asia. Our direct genomic comparisons indicate likely differences in dispersal ecology in these species, despite their phylogenetic proximity, broadly sympatric distributions and similar use of human transport to disperse. Our findings will assist biosecurity operations that aim to trace the source of invasive material and for biocontrol operations that benefit from matching genetic backgrounds of released and local populations. Fig 1. Sampling locations of Aedes aegypti and Aedes albopictus.White lines indicate density of shipping routes. The map uses a Mollweide projection with a central meridian of 120°E. The map was produced in ARCMAP 10.5.1 using shipping route data made available from Halpern et al. [36]. Sampling locations are indicated by letters and are described in Tables 1 and 2.

Incursion pathways of the Asian tiger mosquito (Aedes albopictus) into Australia contrast sharply with those of the yellow fever mosquito (Aedes aegypti)

“…aegypti in Schmidt et al 8 (76%), which is likely in part due to this study using a more conservative cut-off for assignment than used in Schmidt et al 8 (posterior probability > 0.5 and relative probability > 2). The methodology here proved sufficient for confidently assigning among the genetically and geographically close populations of Singapore and Malaysia (FST’ = 0.0251 20 ), with the assignments to Singapore having the highest posterior and relative probabilities of all incursives (Table 1). Likewise, confident assignments were made to Japan, the source of Ae.…”

“…In comparison, two of three Ae. albopictus (SP15-17) detected in fish bins from Hong Kong and one incursive (AP01) detected on cut flowers from China were well-assigned to China, despite the high genetic similarity of Chinese and Taiwanese reference populations (F ST ’ = 0.0197 20 ). Considering these results, the low confidence in specific assignments for incursives SP01-03 and SP11-14 may reflect the absence of reference genotypes from the Americas.…”

“…aegypti both disperse internationally on vessels like ships and aeroplanes, 17–19 analysis of their genetic structure in the Indo-Pacific has indicated that gene flow pathways are different in these species. 20 Likewise, interceptions at New Zealand borders found that most Ae. albopictus were transported as larvae on ships, while most Ae.…”

“…albopictus has been able to colonise distant locations without undergoing ‘stepping stone’ colonisation of intermediate sites. 20,25–27 If gene flow proceeds along different pathways for Ae. albopictus and Ae.…”

“…Nevertheless, the strong differentiation between Indonesian and non-Indonesian populations of Ae. albopictus 20 should allow for assignment between these groups, and thus determine whether Ae. albopictus , like Ae.…”