Gene amplification and microsatellite polymorphism underlie a recent insect host shift

Abstract

Host plant shifts of herbivorous insects may be a first step toward sympatric speciation and can create new pests of agriculturally important crops; however, the molecular mechanisms that mediate this process are poorly understood. Certain races of the polyphagous aphid Myzus persicae have recently adapted to feed on tobacco (Myzus persicae nicotianae) and show a reduced sensitivity to the plant alkaloid nicotine and cross-resistance to neonicotinoids a class of synthetic insecticides widely used for control. Here we show constitutive overexpression of a cytochrome P450 (CYP6CY3) allows tobacco-adapted races of M. persicae to efficiently detoxify nicotine and has preadapted them to resist neonicotinoid insecticides. CYP6CY3, is highly overexpressed in M. persicae nicotianae clones from three continents compared with M. persicae s.s. and expression level is significantly correlated with tolerance to nicotine. CYP6CY3 is highly efficient (compared with the primary human nicotine-metabolizing P450) at metabolizing nicotine and neonicotinoids to less toxic metabolites in vitro and generation of transgenic Drosophila expressing CYP6CY3 demonstrate that it confers resistance to both compounds in vivo. Overexpression of CYP6CY3 results from the expansion of a dinucleotide microsatellite in the promoter region and a recent gene amplification, with some aphid clones carrying up to 100 copies. We conclude that the mutations leading to overexpression of CYP6CY3 were a prerequisite for the host shift of M. persicae to tobacco and that gene amplification and microsatellite polymorphism are evolutionary drivers in insect host adaptation.T oxic secondary metabolites produced by many plant species present barriers to host range expansion by phytophagous insects, and the evolution of mechanisms to circumvent or detoxify these antiherbivore defenses is often a prerequisite for a successful host shift (1-3). Several studies have elucidated the molecular basis of insect adaptation to plant allelochemicals (4-7); however, most of these studies have examined adaptation that has occurred over a long evolutionary time scale and so have been unable to make direct comparisons with nonadapted conspecific races. As a result, identifying the initial genetic changes that enable a host shift has proved elusive. The recent host shift to tobacco (Nicotiana tabacum) by the peach-potato aphid, Myzus persicae, represents one of the few opportunities to study this evolutionary process in action (8). M. persicae is a globally distributed highly polyphagous aphid with a host range of >400 species, including many economically important crop plants (9). Tobacco-adapted races, Myzus persicae nicotianae, are morphologically and genetically differentiated from M. persicae sensu stricto (s.s.), although there are clear examples of recent gene flow between the two taxa (10). M. persicae nicotianae have evolved enhanced tolerance to the pyridine alkaloid nicotine (11), a potent natural insecticide produced by tobacco and other members of the Solanaceae famil...

Adaptation to Nicotine Feeding in Myzus persicae

“…Fecundity of the two M. persicae strains is comparable when feeding on control diet. However, similar to what has been reported with other tobacco-adapted M. persicae (Bass et al, 2014), the red aphid strain was able to survive and reproduce on diets with ~15-fold higher nicotine levels those that are lethal to aphids of the green lineage (Figure 1A). The IC 50 (nicotine concentration that inhibited aphid reproduction by 50%) was determined by linear regression analysis to be 20 μM for the green and 330 μM for the red M. persicae lineage.…”

“…Several tobacco-adapted lineages of M. persicae have genomic increases in the copy number of CYP6CY3 , which encodes a nicotine-detoxifying cytochrome P450 enzyme (Bass et al, 2014; Puinean et al, 2010). Similarly, nicotine resistance in Bemisia tabaci (whitefly) and Manduca sexta (tobacco hornworm) is associated with specific cytochrome P450 detoxifying enzymes (Nauen and Denholm, 2005; Snyder and Feyereisen, 1993).…”

Differences in learning and memory of host plant features between specialist and generalist phytophagous insects

“…Other mechanisms such as upregulation of detoxification-related genes may be also participating in this specialization (Bass et al, 2013). Here, we have identified differences in gene expression of mpfor, a gene related to learning and putatively promoting ecological specialization.…”

Pharmacogenomic Biomarkers for Improved Drug Therapy—Recent Progress and Future Developments

“…Pyriproxyfen Resistance due to 81-fold induction of CYP4G61 expression [15] Honey bee (Apis mellifera) CYP9Q1, CYP9Q2, CYP9Q3 Tau-fluvalinate and coumaphos Resistance due to CYP9Q induction [16] Pollen beetle (Meligethes aeneus) CYP6BQ23 Pyrethroid Up to 900-fold overexpression of CYP6BQ23 conveys pyrethroid resistance [17] Green peach aphid (Myzus persicae) CYP6CY3 Nicotine 100-fold amplification of the CYP6CY3 gene allows the insect to feed on the tobacco plant [18] Homo sapiens CYP2D6 Plant alkaloids Dietary selection for alleles with amplifications of the functional CYP2D6 gene [19] …”