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    Spatial population genomics of a recent mosquito invasion
    Schmidt, TL ; Swan, T ; Chung, J ; Karl, S ; Demok, S ; Yang, Q ; Field, MA ; Muzari, MO ; Ehlers, G ; Brugh, M ; Bellwood, R ; Horne, P ; Burkot, TR ; Ritchie, S ; Hoffmann, AA (WILEY, 2021-03)
    Population genomic approaches can characterize dispersal across a single generation through to many generations in the past, bridging the gap between individual movement and intergenerational gene flow. These approaches are particularly useful when investigating dispersal in recently altered systems, where they provide a way of inferring long-distance dispersal between newly established populations and their interactions with existing populations. Human-mediated biological invasions represent such altered systems which can be investigated with appropriate study designs and analyses. Here we apply temporally restricted sampling and a range of population genomic approaches to investigate dispersal in a 2004 invasion of Aedes albopictus (the Asian tiger mosquito) in the Torres Strait Islands (TSI) of Australia. We sampled mosquitoes from 13 TSI villages simultaneously and genotyped 373 mosquitoes at genome-wide single nucleotide polymorphisms (SNPs): 331 from the TSI, 36 from Papua New Guinea (PNG) and four incursive mosquitoes detected in uninvaded regions. Within villages, spatial genetic structure varied substantially but overall displayed isolation by distance and a neighbourhood size of 232-577. Close kin dyads revealed recent movement between islands 31-203 km apart, and deep learning inferences showed incursive Ae. albopictus had travelled to uninvaded regions from both adjacent and nonadjacent islands. Private alleles and a co-ancestry matrix indicated direct gene flow from PNG into nearby islands. Outlier analyses also detected four linked alleles introgressed from PNG, with the alleles surrounding 12 resistance-associated cytochrome P450 genes. By treating dispersal as both an intergenerational process and a set of discrete events, we describe a highly interconnected invasive system.
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    Genetic stability of Aedes aegypti populations following invasion by wMel Wolbachia
    Lau, M-J ; Schmidt, TL ; Yang, Q ; Chung, J ; Sankey, L ; Ross, PA ; Hoffmann, AA (BMC, 2021-12-14)
    BACKGROUND: Wolbachia wMel is the most commonly used strain in rear and release strategies for Aedes aegypti mosquitoes that aim to inhibit the transmission of arboviruses such as dengue, Zika, Chikungunya and yellow fever. However, the long-term establishment of wMel in natural Ae. aegypti populations raises concerns that interactions between Wolbachia wMel and Ae. aegypti may lead to changes in the host genome, which could affect useful attributes of Wolbachia that allow it to invade and suppress disease transmission. RESULTS: We applied an evolve-and-resequence approach to study genome-wide genetic changes in Ae. aegypti from the Cairns region, Australia, where Wolbachia wMel was first introduced more than 10 years ago. Mosquito samples were collected at three different time points in Gordonvale, Australia, covering the phase before (2010) and after (2013 and 2018) Wolbachia releases. An additional three locations where Wolbachia replacement happened at different times across the last decade were also sampled in 2018. We found that the genomes of mosquito populations mostly remained stable after Wolbachia release, with population differences tending to reflect the geographic location of the populations rather than Wolbachia infection status. However, outlier analysis suggests that Wolbachia may have had an influence on some genes related to immune response, development, recognition and behavior. CONCLUSIONS: Ae. aegypti populations remained geographically distinct after Wolbachia wMel releases in North Australia despite their Wolbachia infection status. At some specific genomic loci, we found signs of selection associated with Wolbachia, suggesting potential evolutionary impacts can happen in the future and further monitoring is warranted.
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    The mitogenome of Halotydeus destructor (Tucker) and its relationships with other trombidiform mites as inferred from nucleotide sequences and gene arrangements
    Thia, JA ; Young, ND ; Korhnen, PK ; Yang, Q ; Gasser, RB ; Umina, PA ; Hoffmann, AA (WILEY, 2021-10)
    The redlegged earth mite, Halotydeus destructor (Tucker, 1925: Trombidiformes, Eupodoidea, Penthaleidae), is an invasive mite species. In Australia, this mite has become a pest of winter pastures and grain crops. We report the complete mitogenome for H. destructor, the first to represent the family Penthaleidae, superfamily Eupodoidea. The mitogenome of H. destructor is 14,691 bp in size, and has a GC content of 27.87%, 13 protein-coding genes, two rRNA genes, and 22 tRNA genes. We explored evolutionary relationships of H. destructor with other members of the Trombidiformes using phylogenetic analyses of nucleotide sequences and the order of protein-coding and rRNA genes. We found strong, consistent support for the superfamily Tydeoidea being the sister taxon to the superfamily Eupodoidea based on nucleotide sequences and gene arrangements. Moreover, the gene arrangements of Eupodoidea and Tydeoidea are not only identical to each other but also identical to that of the hypothesized arthropod ancestor, showing a high level of conservatism in the mitogenomic structure of these mite superfamilies. Our study illustrates the utility of gene arrangements for providing complementary information to nucleotide sequences with respect to inferring the evolutionary relationships of species within the order Trombidiformes. The mitogenome of H. destructor provides a valuable resource for further population genetic studies of this important agricultural pest. Given the co-occurrence of closely related, morphologically similar Penthaleidae mites with H. destructor in the field, a complete mitogenome provides new opportunities to develop metabarcoding tools to study mite diversity in agro-ecosystems. Moreover, the H. destructor mitogenome fills an important taxonomic gap that will facilitate further study of trombidiform mite evolution.
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    Origin of resistance to pyrethroids in the redlegged earth mite (Halotydeus destructor) in Australia: repeated local evolution and migration
    Yang, Q ; Umina, PA ; Rasic, G ; Bell, N ; Fang, J ; Lord, A ; Hoffmann, AA (JOHN WILEY & SONS LTD, 2020-02)
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    Migration trajectories of the diamondback moth Plutella xylostella in China inferred from population genomic variation
    Chen, M-Z ; Cao, L-J ; Li, B-Y ; Chen, J-C ; Gong, Y-J ; Yang, Q ; Schmidt, TL ; Yue, L ; Zhu, J-Y ; Li, H ; Chen, X-X ; Hoffmann, AA ; Wei, S-J (JOHN WILEY & SONS LTD, 2021-04)
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    Anthropogenic and natural barriers affect genetic connectivity in an Alpine butterfly
    Trense, D ; Schmidt, TL ; Yang, Q ; Chung, J ; Hoffmann, AA ; Fischer, K (WILEY, 2021-01)
    Dispersal is a key biological process serving several functions including connectivity among populations. Habitat fragmentation caused by natural or anthropogenic structures may hamper dispersal, thereby disrupting genetic connectivity. Investigating factors affecting dispersal and gene flow is important in the current era of anthropogenic global change, as dispersal comprises a vital part of a species' resilience to environmental change. Using finescale landscape genomics, we investigated gene flow and genetic structure of the Sooty Copper butterfly (Lycaena tityrus) in the Alpine Ötz valley system in Austria. We found surprisingly high levels of gene flow in L. tityrus across the region. Nevertheless, ravines, forests, and roads had effects on genetic structure, while rivers did not. The latter is surprising as roads and rivers have a similar width and run largely in parallel in our study area, pointing towards a higher impact of anthropogenic compared with natural linear structures. Additionally, we detected eleven loci potentially under thermal selection, including ones related to membranes, metabolism, and immune function. This study demonstrates the usefulness of molecular approaches in obtaining estimates of dispersal and population processes in the wild. Our results suggest that, despite high gene flow in the Alpine valley system investigated, L. tityrus nevertheless seems to be vulnerable to anthropogenically-driven habitat fragmentation. With anthropogenic rather than natural linear structures affecting gene flow, this may have important consequences for the persistence of species such as the butterfly studied here in altered landscapes.
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    Wolbachia Genome Stability and mtDNA Variants in Aedes aegypti Field Populations Eight Years after Release
    Huang, B ; Yang, Q ; Hoffmann, AA ; Ritchie, SA ; van den Hurk, AF ; Warrilow, D (CELL PRESS, 2020-10-23)
    A dengue suppression strategy based on release of Aedes aegypti mosquitoes infected with the bacterium Wolbachia pipientis is being trialed in many countries. Wolbachia inhibits replication and transmission of dengue viruses. Questions remain regarding the long-term stability of virus-suppressive effects. We sequenced the Wolbachia genome and analyzed Ae. aegypti mitochondrial DNA markers isolated from mosquitoes sampled 2-8 years after releases in the greater Cairns region, Australia. Few changes were detected when Wolbachia genomes of field mosquitoes were compared with Wolbachia genomes of mosquitoes obtained soon after initial releases. Mitochondrial variants associated with the initial Wolbachia release stock are now the only variants found in release sites, highlighting maternal leakage as a possible explanation for rare Wolbachia-negative mosquitoes and not migration from non-release areas. There is no evidence of changes in the Wolbachia genome that indicate selection against its viral-suppressive effects or other phenotypes attributable to infection with the bacterium.
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    Heatwaves cause fluctuations in wMel Wolbachia densities and frequencies in Aedes aegypti
    Ross, PA ; Axford, JK ; Yang, Q ; Staunton, KM ; Ritchie, SA ; Richardson, KM ; Hoffmann, AA ; Kohl, A (PUBLIC LIBRARY SCIENCE, 2020-01)
    Aedes aegypti mosquitoes infected with the wMel strain of Wolbachia are being released into natural mosquito populations in the tropics as a way of reducing dengue transmission. High temperatures adversely affect wMel, reducing Wolbachia density and cytoplasmic incompatibility in some larval habitats that experience large temperature fluctuations. We monitored the impact of a 43.6°C heatwave on the wMel infection in a natural population in Cairns, Australia, where wMel was first released in 2011 and has persisted at a high frequency. Wolbachia infection frequencies in the month following the heatwave were reduced to 83% in larvae sampled directly from field habitats and 88% in eggs collected from ovitraps, but recovered to be near 100% four months later. Effects of the heatwave on wMel appeared to be stage-specific and delayed, with reduced frequencies and densities in field-collected larvae and adults reared from ovitraps but higher frequencies in field-collected adults. Laboratory experiments showed that the effects of heatwaves on cytoplasmic incompatibility and density are life stage-specific, with first instar larvae being the most vulnerable to temperature effects. Our results indicate that heatwaves in wMel-infected populations will have only temporary effects on Wolbachia frequencies and density once the infection has established in the population. Our results are relevant to ongoing releases of wMel-infected Ae. aegypti in several tropical countries.
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    An elusive endosymbiont: Does Wolbachia occur naturally in Aedes aegypti?
    Ross, PA ; Callahan, AG ; Yang, Q ; Jasper, M ; Arif, MAK ; Afizah, AN ; Nazni, WA ; Hoffmann, AA (Wiley, 2020-02)
    Wolbachia are maternally inherited endosymbiotic bacteria found within many insect species. Aedes mosquitoes experimentally infected with Wolbachia are being released into the field for Aedes‐ borne disease control. These Wolbachia infections induce cytoplasmic incompatibility which is used to suppress populations through incompatible matings or replace populations through the reproductive advantage provided by this mechanism. However, the presence of naturally occurring Wolbachia in target populations could interfere with both population replacement and suppression programs depending on the compatibility patterns between strains. Aedes aegypti were thought to not harbor Wolbachia naturally but several recent studies have detected Wolbachia in natural populations of this mosquito. We therefore review the evidence for natural Wolbachia infections in A. aegypti to date and discuss limitations of these studies. We draw on research from other mosquito species to outline the potential implications of natural Wolbachia infections in A. aegypti for disease control. To validate previous reports, we obtained a laboratory population of A. aegypti from New Mexico, USA, that harbors a natural Wolbachia infection, and we conducted field surveys in Kuala Lumpur, Malaysia, where a natural Wolbachia infection has also been reported. However, we were unable to detect Wolbachia in both the laboratory and field populations. Because the presence of naturally occurring Wolbachia in A. aegypti could have profound implications for Wolbachia ‐based disease control programs, it is important to continue to accurately assess the Wolbachia status of target Aedes populations.