Quantitative trait loci mapping reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Biological invasions offer a unique opportunity to investigate evolution over contemporary timescales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species' invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4493 SNPs) and paired this with phenotypic data from an F2 mapping population (n = 336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger, and more tightly linked alleles should underlie rapid local adaptation during invasion, particularly when divergently adapting populations experience high levels of gene flow

Uncovering the genomic basis of an extraordinary plant invasion

Invasive species are a key driver of the global biodiversity crisis, but the drivers of invasiveness, including the role of pathogens, remain debated. We investigated the genomic basis of invasiveness in Ambrosia artemisiifolia (common ragweed), introduced to Europe in the late 19th century, by resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In invasive European populations, we found selection signatures in defense genes and lower prevalence of disease-inducing plant pathogens. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from specific microbial enemies likely favored the plant's remarkable success as an invasive species.Peer reviewe

Genomic Tools in Biological Invasions: Current State and Future Frontiers

Human activities are accelerating rates of biological invasions and climate-driven range expansions globally, yet we understand little of how genomic processes facilitate the invasion process. Although most of the literature has focused on underlying phenotypic correlates of invasiveness, advances in genomic technologies are showing a strong link between genomic variation and invasion success. Here, we consider the ability of genomic tools and technologies to (i) inform mechanistic understanding of biological invasions and (ii) solve real-world issues in predicting and managing biological invasions. For both, we examine the current state of the field and discuss how genomics can be leveraged in the future. In addition, we make recommendations pertinent to broader research issues, such as data sovereignty, metadata standards, collaboration, and science communication best practices that will require concerted efforts from the global invasion genomics community

The quantitative genetics of insecticide resistance in Drosophila melanogaster

© 2019 Paul BattlayWhile understanding insecticide resistance in Drosophila melanogaster is informative for controlling pest insects that threaten agricultural yields and vector deadly diseases, it also serves as a powerful model of microevolution which can be interrogated with an exceptionally powerful genetic toolkit. The Drosophila Genetic Reference Panel (DGRP) provides the opportunity to study population-genetic signatures of natural selection in individuals that can be repeatedly measured for a range of phenotypes. In this work, genomic and transcriptomic data from the DGRP are compared with phenotypes from nine insecticidal compounds against the background of genome-wide signals of selection. The two most prominent signatures of selection in the population are attributable to insecticides from a single, widely-used chemical class, the organophosphates. Evidence suggests that insecticide-based selection is limited to these two loci, however the genetic bases of insecticide phenotypes appear to be complex. Insecticide-associated variation includes both structural effects through amino acid substitution and chimeric gene formation, and regulatory effects on transcript abundance by cis- and trans-acting factors. Resistance mechanisms exhibiting pleiotropic effects on insecticides from different chemical classes is found to be rare; one such case is correlated with constitutive, modular regulation of oxidative stress-related transcripts, the genetic basis of which is mapped to multiple trans-acting factors. Comparisons of the results from the DGRP with diverse population genomics data suggests that the outcomes of these analyses are applicable to populations of D. melanogaster worldwide

The molecular evolution of cytochrome P450 genes within and between Drosophila species

We map 114 gene gains and 74 gene losses in the P450 gene family across the phylogeny of 12 Drosophila species by examining the congruence of gene trees and species trees. Although the number of P450 genes varies from 74 to 94 in the species examined, we infer that there were at least 77 P450 genes in the ancestral Drosophila genome. One of the most striking observations in the data set is the elevated loss of P450 genes in the Drosophila sechellia lineage. The gain and loss events are not evenly distributed among the P450 genes—with 30 genes showing no gene gains or losses whereas others show as many as 20 copy number changes among the species examined. The P450 gene clades showing the fewest number of gene gain and loss events tend to be those evolving with the most purifying selection acting on the protein sequences, although there are exceptions, such as the rapid rate of amino acid replacement observed in the single copy phantom (Cyp306a1) gene. Within D. melanogaster, we observe gene copy number polymorphism in ten P450 genes including multiple cases of interparalog chimeras. Nonallelic homologous recombination (NAHR) has been associated with deleterious mutations in humans, but here we provide a second possible example of an NAHR event in insect P450s being adaptive. Specifically, we find that a polymorphic Cyp12a4/Cyp12a5 chimera correlates with resistance to an insecticide. Although we observe such interparalog exchange in our within-species data sets, we have little evidence of it between species, raising the possibility that such events may occur more frequently than appreciated but are masked by subsequent sequence change

Structural Variants and Selective Sweep Foci Contribute to Insecticide Resistance in the Drosophila Genetic Reference Panel.

Patterns of nucleotide polymorphism within populations of Drosophila melanogaster suggest that insecticides have been the selective agents driving the strongest recent bouts of positive selection. However, there is a need to explicitly link selective sweeps to the particular insecticide phenotypes that could plausibly account for the drastic selective responses that are observed in these non-target insects. Here, we screen the Drosophila Genetic Reference Panel with two common insecticides; malathion (an organophosphate) and permethrin (a pyrethroid). Genome-wide association studies map survival on malathion to two of the largest sweeps in the D. melanogaster genome; Ace and Cyp6g1 Malathion survivorship also correlates with lines which have high levels of Cyp12d1, Jheh1 and Jheh2 transcript abundance. Permethrin phenotypes map to the largest cluster of P450 genes in the Drosophila genome, however in contrast to a selective sweep driven by insecticide use, the derived allele seems to be associated with susceptibility. These results underscore previous findings that highlight the importance of structural variation to insecticide phenotypes: Cyp6g1 exhibits copy number variation and transposable element insertions, Cyp12d1 is tandemly duplicated, the Jheh loci are associated with a Bari1 transposable element insertion, and a Cyp6a17 deletion is associated with susceptibility

Dissecting the Insect Metabolic Machinery Using Twin Ion Mass Spectrometry: A Single P450 Enzyme Metabolizing the Insecticide Imidacloprid <i>in Vivo</i>

Insecticide resistance is one of the most prevalent examples of anthropogenic genetic change, yet our understanding of metabolic-based resistance remains limited by the analytical challenges associated with rapidly tracking the <i>in vivo</i> metabolites of insecticides at nonlethal doses. Here, using twin ion mass spectrometry analysis of the extracts of whole <i>Drosophila larvae</i> and excreta, we show that (i) eight metabolites of the neonicotinoid insecticide, imidacloprid, can be detected when formed by susceptible larval genotypes and (ii) the specific overtranscription of a single gene product, <i>Cyp6g1</i>, associated with the metabolic resistance to neonicotinoids, results in a significant increase in the formation of three imidacloprid metabolites that are formed in C–H bond activation reactions; that is, <i>Cyp6g1</i> is directly linked to the enhanced metabolism of imidacloprid <i>in vivo</i>. These results establish a rapid and sensitive method for dissecting the metabolic machinery of insects by directly linking single gene products to insecticide metabolism

Large haploblocks underlie rapid adaptation in the invasive weed Ambrosia artemisiifolia

Ambrosia artemisiifolia is an invasive weed and primary cause of pollen-induced hayfever. Here, the authors report its chromosome-level phased genome assembly, examine genome-wide variation among modern and historic accessions, and identify large haploblocks underling rapid adaptation