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Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe.

ABSTRACT: BACKGROUND:In the last four decades, the Asian tiger mosquito, Aedes albopictus, vector of several human arboviruses, has spread from its native range in South-East Asia to all over the world, largely through the transportation of its eggs via the international trade in used tires. Albania was the first country invaded in Europe in 1979, followed by Italy in 1990 and other Mediterranean countries after 2000. METHODS/PRINCIPAL FINDINGS:We here inferred the invasion history and migration patterns of Ae. albopictus in Italy (today the most heavily-infested country in Europe), Greece and Albania, by analyzing a panel of >100,000 single nucleotide polymorphisms (SNPs) obtained by sequencing of double-digest Restriction site-Associated DNA (ddRADseq). The obtained dataset was combined with samples previously analyzed from both the native and invasive range worldwide to interpret the results using a broader spatial and historical context. The emerging evolutionary scenario complements the results of other studies in showing that the extraordinary worldwide expansion of Ae. albopictus has occurred thanks to multiple independent invasions by large numbers of colonists from multiple geographic locations in both native and previously invaded areas, consistently with the role of used tires shipments to move large numbers of eggs worldwide. By analyzing mosquitoes from nine sites across ~1,000-km transect in Italy, we were able to detect a complex interplay of drift, isolation by distance mediated divergence, and gene flow in shaping the species very recent invasion and range expansion, suggesting overall high connectivity, likely due to passive transportation of adults via ground transportation, as well as specific adaptations to local conditions. CONCLUSIONS/SIGNIFICANCE:Results contribute to characterize one of the most successful histories of animal invasion, and could be used as a baseline for future studies to track epidemiologically relevant characters (e.g. insecticide resistance).

SUBMITTER: Pichler V

PROVIDER: S-EPMC6705758 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe.

Pichler Verena V Kotsakiozi Panayiota P Caputo Beniamino B Serini Paola P Caccone Adalgisa A Della Torre Alessandra A

PLoS neglected tropical diseases 20190822 8

<h4>Background</h4>In the last four decades, the Asian tiger mosquito, Aedes albopictus, vector of several human arboviruses, has spread from its native range in South-East Asia to all over the world, largely through the transportation of its eggs via the international trade in used tires. Albania was the first country invaded in Europe in 1979, followed by Italy in 1990 and other Mediterranean countries after 2000.<h4>Methods/principal findings</h4>We here inferred the invasion history and migr ...[more]

PMID: 31437154

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Project description:BACKGROUND: Levels of differentiation among populations depend both on demographic and selective factors: genetic drift and local adaptation increase population differentiation, which is eroded by gene flow and balancing selection. We describe here the genomic distribution and the properties of genomic regions with unusually high and low levels of population differentiation in humans to assess the influence of selective and neutral processes on human genetic structure. METHODS: Individual SNPs of the Human Genome Diversity Panel (HGDP) showing significantly high or low levels of population differentiation were detected under a hierarchical-island model (HIM). A Hidden Markov Model allowed us to detect genomic regions or islands of high or low population differentiation. RESULTS: Under the HIM, only 1.5% of all SNPs are significant at the 1% level, but their genomic spatial distribution is significantly non-random. We find evidence that local adaptation shaped high-differentiation islands, as they are enriched for non-synonymous SNPs and overlap with previously identified candidate regions for positive selection. Moreover there is a negative relationship between the size of islands and recombination rate, which is stronger for islands overlapping with genes. Gene ontology analysis supports the role of diet as a major selective pressure in those highly differentiated islands. Low-differentiation islands are also enriched for non-synonymous SNPs, and contain an overly high proportion of genes belonging to the 'Oncogenesis' biological process. CONCLUSIONS: Even though selection seems to be acting in shaping islands of high population differentiation, neutral demographic processes might have promoted the appearance of some genomic islands since i) as much as 20% of islands are in non-genic regions ii) these non-genic islands are on average two times shorter than genic islands, suggesting a more rapid erosion by recombination, and iii) most loci are strongly differentiated between Africans and non-Africans, a result consistent with known human demographic history.

Project description:The Asian tiger mosquito Aedes albopictus, native to South East Asia, is listed as one of the worst invasive vector species worldwide. In Europe the species is currently restricted to Southern Europe, but due to the ongoing climate change, Ae. albopictus is expected to expand its potential range further northwards. In addition to modelling the habitat suitability for Ae. albopictus under current and future climatic conditions in Europe by means of the maximum entropy approach, we here focused on the drivers of the habitat suitability prediction. We explored the most limiting factors for Aedes albopictus in Europe under current and future climatic conditions, a method which has been neglected in species distribution modelling so far. Ae. albopictus is one of the best-studied mosquito species, which allowed us to evaluate the applied Maxent approach for most limiting factor mapping. We identified three key limiting factors for Ae. albopictus in Europe under current climatic conditions: winter temperature in Eastern Europe, summer temperature in Southern Europe. Model findings were in good accordance with commonly known establishment thresholds in Europe based on climate chamber experiments and derived from the geographical distribution of the species. Under future climatic conditions low winter temperature were modelled to remain the most limiting factor in Eastern Europe, whereas in Central Europe annual mean temperature and summer temperatures were modelled to be replaced by summer precipitation, respectively, as most limiting factors. Changes in the climatic conditions in terms of the identified key limiting factors will be of great relevance regarding the invasive potential of the Ae. albopictus. Thus, our results may help to understand the key drivers of the suggested range expansion under climate change and may help to improve monitoring programmes. The applied approach of investigating limiting factors has proven to yield valuable results and may also provide valuable insights into the drivers of the prediction of current and future distribution of other species. This might be particularly interesting for other vector species that are of increasing public health concerns.

Project description:BackgroundThe exotic invasive tiger mosquito, Aedes albopictus, appeared in southern Switzerland in 2003. The spread of the mosquito has been surveyed constantly since then, and an integrated vector management (IVM) has been implemented to control its numbers. The control measures focus on the aquatic phase of the mosquito with removal of breeding sites and applications of larvicides in public areas whereas private areas are reached through extensive public information campaigns. Here, we evaluated the efficacy of the IVM.MethodsSince all the municipalities with Ae. albopictus in southern Switzerland are currently implementing the IVM, Italian municipalities just across the Swiss-Italian border, where Ae. albopictus is present but no coordinated intervention programme is in place, served as control. Ovitraps and adult female traps were used to measure mosquito abundance in 2019. Generalised mixed-effects models were used to model the numbers of Ae. albopictus eggs and adult females collected. These numbers of Ae. albopictus eggs were compared to the numbers of eggs collected in 2012 and 2013 in a previous assessment of the IVM, using a hurdle model.ResultsMean numbers of Ae. albopictus eggs and adult females in 2019 were consistently higher in the municipalities not following an IVM programme. In these municipalities, there were about four times (3.8) more eggs than in the municipalities implementing an IVM programme. Also, the numbers of eggs and adult females increased steadily from the beginning of the Ae. albopictus reproductive season, reaching a peak in August. In contrast, the increase in numbers of Ae. albopictus was much more contained in the municipalities implementing an IVM programme, without reaching an evident peak. Comparison with data from 2012 and 2013 indicates that the gap between intervention and non-intervention areas may have almost doubled in the past 6 years.ConclusionsThe results of the survey strongly support the efficacy of the IVM programme implemented in southern Switzerland compared to municipalities without defined control measures. With the constant implementation of an IVM, it appears possible to contain the numbers of Ae. albopictus at a manageable level, reducing the nuisance for the human population and the risk of arbovirus epidemics.

Project description:BackgroundIn eukaryotic organisms, Piwi-interacting RNAs (piRNAs) control the activities of mobile genetic elements and ensure genome maintenance. Recent evidence indicates that piRNAs are involved in multiple biological pathways, including transcriptional regulation of protein-coding genes, sex determination and even interactions between host and pathogens. Aedes albopictus is a major invasive species that transmits a number of viral diseases in humans. Ae. albopictus has the largest genome and the highest abundance of repetitive sequences when compared with members that belong to Culicidae with a published genome. Analysis of piRNA profiles will provide a developmental and evolutionary perspective on piRNAs in Ae. albopictus.MethodspiRNAs were identified and characterized during the development of Ae. albopictus, and piRNA expression patterns in adult males and females as well as sugar-fed females and blood-fed females were compared.ResultsOur results reveal that, despite the large genome size of Ae. albopictus, the piRNA pool of Ae. albopictus (1.2 × 107) is smaller than those of Aedes aegypti (1.7 × 107) and Drosophila melanogaster (1.6 × 107). In Ae. albopictus, piRNAs displayed the highest abundance at the embryo stage and the lowest abundance at the pupal stage. Approximately 50 % of the piRNAs mapped to intergenic regions with no known functions. Approximately 30 % of the piRNAs mapped to repetitive elements, and 77.69 % of these repeat-derived piRNAs mapped to Class I TEs; 45.42 % of the observed piRNA reads originated from piRNA clusters, and most of the top 10 highest expressed piRNA clusters and 100 highest expressed piRNAs from each stage displayed biased expression patterns across the developmental stages. All anti-sense-derived piRNAs displayed a preference for uridine at the 5' end; however, the sense-derived piRNAs showed adenine bias at the tenth nucleotide position and a typical ping-pong signature, suggesting that the biogenesis of piRNAs was conserved throughout development. Our results also show that 962 piRNAs displayed sex-biased expression, and 522 piRNAs showed higher expression in the blood-fed females than in the sugar-fed females.ConclusionsOur results suggest that piRNAs, aside from silencing transposable elements in Ae. albopictus, may have a role in other biological pathways.

Project description: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 investigated patterns of genome-wide genetic differentiation to compare pathways of invasion and ongoing gene flow in both species, and to compare invasive and native-range populations of 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 representing potential native-range populations and potential cryptic subspeciation 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 the situation in Ae. aegypti, we found evidence of long-distance Ae. albopictus colonisation events, including colonisation of Mauritius from East Asia and of Fiji from Southeast Asia. These direct genomic comparisons indicate likely differences in dispersal ecology in these species, despite their broadly sympatric distributions and similar use of human transport to disperse. Our findings will assist biosecurity operations to trace the source of invasive material and for biocontrol operations that benefit from matching genetic backgrounds of released and local populations.

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Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe.

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Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe.

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