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Rane, R.

Publications and source records attributed to Rane, R..

7 recordsLinked to original sources

Strong reproductive isolation among sympatric lineages of an international mosquito pest

Background: Reproductive isolation describes the degree to which genetic differences among populations reduce the level of neutral gene flow between them. Genomic approaches are currently showing great utility for identifying reproductive isolation between sympatric, morphologically indistinct populations, where hybridisation and introgression may yet be common. Here we use population genomic approaches and a chromosome-level reference assembly to uncover three highly differentiated, cryptic lineages of Aedes notoscriptus, an Australian mosquito disease vector that has invaded New Zealand (c. 1920) and California (c. 2014). Results: We identified a single lineage (Noto1) that was the source of the New Zealand and Californian invasions, and this lineage was also distributed across much of Australia including the Greater Melbourne region where it was sympatric with a second lineage (Noto2). Although Victorian Noto1 and Noto2 were frequently sampled co-locally, hybrids were observed less frequently than expected under random mating, and admixture levels were low, suggestive of selection against hybrids. A bottleneck observed in Victorian Noto1 suggests that Noto1 may have recently expanded its range into the Greater Melbourne region. We also identified a massive structural variant (~25 Mbp; ~10% of chromosome size) in Noto2 that was segregating at intermediate frequencies across the Greater Melbourne region but was fixed in Noto1. Conclusion: Together, these results identify key genetic differences between cryptic lineages of this international disease vector that warrant further investigation given potential differences in vector competence.

evolutionary biology↗

Populations of the Australian saltmarsh mosquito Aedes vigilax vary between panmixia and temporally stable local genetic structure

Pest management programs can operate more effectively when movement patterns of target species are known. As individual insects are difficult to track, genomic data can instead be used to infer movement patterns based on pest population structure and connectivity. These data can also provide critical information about cryptic taxa relevant to management. Here we present the first genomic investigation of Aedes vigilax, the Australian saltmarsh mosquito, a major arbovirus vector across Australasia. We used a ddRAD pool-seq approach and a draft genome assembly to investigate genetic variation in 60 Ae. vigilax pools from across Australia but with a focus on urban Newcastle and Sydney, NSW. There was strong genetic structure between samples from the west and east coasts of Australia, and additional structure that differentiated east coast populations. Within Newcastle and Sydney, contrasting patterns of genetic structure were evident. In Newcastle, there was no differentiation among subregions up to 60 km apart. In Sydney, samples from one urban subregion were differentiated from others < 3 km apart, and this structure was stable across sampling years. Heterozygosity and Tajimas D indicated no bottlenecks in Newcastle or Sydney populations, suggesting this structure represents a gene flow barrier. Nuclear differentiation patterns contrast with previous mtDNA data indicating two COI clades in the east coast, one of which was also present in Western Australia. The panmixia over 60 km across the Newcastle region corroborates previous field observations of high dispersal capacity in this mosquito. These findings indicate specific challenges that may hinder local suppression strategies for this species.

evolutionary biology↗

Chromosome structural rearrangements in invasive haplodiploid ambrosia beetles revealed by the genomes of Euwallacea fornicatus and Euwallacea similis (Coleoptera, Curculionidae, Scolytinae)

Bark and ambrosia beetles are among the most ecologically and economically damaging introduced plant pests worldwide, with life history traits including polyphagy, haplodiploidy, inbreeding polygyny and symbiosis with fungi contributing to their dispersal and impact. Species vary in host tree ecologies, with many attacking stressed or recently dead trees, such as the globally distributed E. similis (Ferrari). Other species, like the Polyphagous Shot Hole Borer (PSHB) Euwallacea fornicatus (Eichhoff), can attack over 680 host plants and is causing considerable economic damage in several countries worldwide. Despite their notoriety, publicly accessible genomic resources for Euwallacea Hopkins species are scarce, hampering better understanding of their invasive capabilities as well as modern control measures, surveillance and management. Using a combination of long and short read sequencing platforms we assembled and annotated high quality (BUSCO > 98% complete) chromosome level genomes for these species. Comparative macro-synteny analysis showed an increased number of chromosomes in the haplodiploid inbreeding species of Euwallacea compared to diploid outbred species, due to fission events. This suggests that life history traits can impact chromosome structure. Further, the genome of E. fornicatus had a higher relative proportion of repetitive elements, up to 17% more, than E. similis. Additionally, metagenomic assembly pipelines identified microbiota associated with both species including Fusarium fungal symbionts and a novel Wolbachia strain. These novel genomes of haplodiploid inbreeding species will contribute to the understanding of how life history traits are related to their evolution and will contribute to the management of these invasive pests. SignificanceScolytinae are significant forestry pests around the world and commonly translocated due to human trade of wood and plant products. Life history traits including inbreeding and haplodiploidy are attributed to their successful establishment in novel environments. Euwallacea fornicatus is widely distributed and attacks a wide variety of live host trees. This study reports the genome of this species and for, E. similis, which colonises dead host trees. The genome assemblies presented herein are highly complete and scaffolded to pseudo-chromosomal level. Comparative analyses of these genomes and of other Scolytinae highlight significant chromosomal rearrangements between haplodiploid inbreeding Euwallacea and diploid outbreeding scolytinae species. Higher relative proportions of transposable elements were identified E. fornicatus, which may promote the species ability to attack live host trees. These genomes are the first for haplodiploid beetles and will contribute to the understanding of evolution of life history traits and the management of invasive insects.

genomics↗

Complex multiple introductions drive fall armyworm invasions into Asia and Australia

The fall armyworm (FAW) Spodoptera frugiperda is thought to have undergone a rapid west-to-east spread since 2016 when it was first identified in western Africa. Between 2018 and 2020, it was also recorded from South Asia (SA), Southeast Asia (SEA), East Asia (EA), and Pacific/Australia (PA). Population genomic analyses enabled the understanding of pathways, population sources, and gene flow in this notorious agricultural pest species. Using neutral single nucleotide polymorphic (SNP) DNA markers, we detected genome introgression that suggested most populations were overwhelmingly C- and R-strain hybrids. SNP and mitochondrial DNA markers identified multiple introductions that were most parsimoniously explained by anthropogenic-assisted spread, i.e., associated with international trade of live/fresh plants and plant products, and involved bridgehead populations in countries to enable successful pest establishment in neighbouring countries. Distinct population genomic signatures between Myanmar and China do not support the African origin spread nor the Myanmar source population to China hypotheses. Significant genetic differentiation between populations from different Australian states supported multiple pathways involving distinct SEA populations. Our study identified Asia as a biosecurity hotspot and a FAW genetic melting pot, and demonstrated the use of genome analysis to disentangle preventable human-assisted pest introductions from unpreventable natural pest spread.

evolutionary biology↗

Urban population structure and local movement ecology of a native Australian mosquito involved in disease transmission

Dispersal is a critical factor in designing successful pest control measures as it determines the rate of movement across target control areas and influences the risk of human exposure to the species and its pathogens. Here we used a fine scale spatial population genomic approach to investigate the dispersal ecology and population structure of Aedes notoscriptus, an important disease transmitting mosquito, on the Mornington Peninsula near Melbourne, Australia. The species is suspected to be involved in the transmission of Mycobacterium ulcerans, the bacterium that causes Buruli ulcer, in this area. We sampled and reared Ae. notoscriptus eggs at two time points from 170 traps up to 5 km apart and generated genomic data from 240 individuals. We also produced a draft genome assembly from a laboratory colony established from mosquitoes sampled near the study area. We found low genetic structure (Fst) and high coancestry throughout the study region. Using genetic data to identify close kin dyads, we found that mosquitoes had moved distances of >1km within a generation, which is further than previously described for this species. A spatial autocorrelation analysis of genetic distances indicated genetic dissimilarity at >4 km separation, a fourfold higher distance than for a comparable population of the dengue mosquito, Ae. aegypti, from Cairns, Australia. These findings point to high mobility of Ae. notoscriptus, highlighting the challenges of localized intervention strategies targeting this species. Further sampling within the same area at two time points 6 and 12 months after initial sampling showed that egg counts were relatively consistent across time, and that spatial variation in egg counts covaried with spatial variation in Wrights neighbourhood size (NS). As NS increases linearly with population density, egg counts may be useful for estimating relative density in Ae. notoscriptus. The results highlight the importance of acquiring species-specific data when planning control measures.

ecology↗

Whole genome sequencing of global Spodoptera frugiperda populations: evidence for complex, multiple introductions across the Old World

Native to the Americas, the invasive Spodoptera frugiperda (fall armyworm; FAW) was reported in West Africa in 2016, followed by chronological order of detections across the Old World and the hypothesis of an eastward Asia expansion. We explored population genomic signatures of American and Old World FAW and identified 12 maternal mitochondrial DNA genome lineages across the invasive range, while from 870 high-quality nuclear single nucleotide polymorphic DNA markers five distinct New World population clusters were identified, broadly reflected their native geographical ranges and absence of host-plant preferences. We identified unique admixed Old World populations, and admixed and non-admixed Asian FAW individuals, all of which suggested multiple introductions underpinned the pests global spread. Directional gene flow from the East into eastern Africa was also detected, in contrast to the west-to-east spread hypothesis. Our study demonstrated population genomic approaches via international partnership to address global emerging pest threats and biosecurity challenges.

genomics↗

Adaptive introgression across semipermeable species boundaries between local Helicoverpa zea and invasive Helicoverpa armigera moths

Hybridization between invasive and native species has raised global concern given the dramatic increase in species range shifts and pest outbreaks due to climate change, development of suitable agroecosystems, and anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013, and more recent populations from 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, admixture proportions were reduced between 2013 and 2017, indicating a decline in hybridization rates. Recent populations also showed shorter introgressed tracks suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for introgression of a single region including an insecticide-resistance allele from the invasive H. armigera into local H. zea, which increased in frequency over time but was localized within the genome. In summary, despite extensive gene-flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression and hybridization, with significant implications for pest management in future population expansions and introductions of novel resistance genes from new invasive H. armigera populations. Author summarySecondary contact occurs when related species with non-overlapping ranges are geographically reunited. Scenarios of secondary contact have increased due to anthropogenic movement of species outside of their native range, often resulting in invasive species that successfully spread and stabilised in the new environment. This is the case for Helicoverpa armigera, a major agricultural pest in the Old World that has recently invaded the Americas, where it reunited with its closest relative, H. zea. While some authors reported hybridisation, and hypothesised about the potential emergence of novel ecotypes and the exchange of pesticide-resistant genes, these outcomes have not been tested yet. We examine these outcomes by sequencing individuals from both species in Brazil, collected in 2013 after outbreaks of H. armigera were reported, and individuals collected during 2017. We discovered that despite hybridisation, these moths have not collapsed into a single species nor formed new ecotypes, and that the species distinctiveness is maintained through selection against most of the foreign genotypes that cross species boundaries. However, we found that hybridisation mediated the rapid acquisition of a H. armigera gene conferring resistance to pyrethroids by H. zea. The overall decline in populations of both species during the interval covered by this study means that our results are likely to reflect the consequences of hybridization events early after invasion, despite the likely ongoing introduction of H. armigera genetic diversity through trade across the South American continent. Our results provide a rare example of adaptive transferral of variation right after invasion and elucidate the dynamics of insecticide resistance evolution in H. zea.

evolutionary biology↗