Changes in insecticide resistance and host range performance of planthoppers artificially selected to feed on resistant rice

Abstract

Host plant resistance has received considerable attention for the management of insect herbivores on crop plants. However, resistance is threatened by the rapid adaptation of target herbivores towards virulence (the ability to survive, develop and damage a host with major resistance genes). This study examines the potential costs and benefits of adaptation for virulence in herbivores. We continuously reared planthoppers, Nilaparvata lugens, on two susceptible and three resistant rice, Oryza sativa, varieties for 20 + generations. We then assessed the performance of selected planthoppers across a range of rice lines with distinct resistance genes. We found that planthoppers with long-term exposure to resistant hosts (particularly IR62 with the Bph3(t) and BPH32 gene loci, and PTB33 with the Bph3(t), BPH32 and BPH26 gene loci) gained virulence against related varieties with the same and different resistance genes, but planthoppers adapted to the resistant host IR65482-4-136-2-2 (BPH10 locus) had reduced performance on phylogenetically distant plants with distinct resistant genes. In choice bioassays, avirulent planthoppers showed marked preferences for susceptible lines, whereas virulent planthoppers were less selective of varieties. We also examined whether virulence was associated with insecticide susceptibility. We tested susceptibility to three insecticides using a topical application method. Populations selectively reared on IR65482-4-136-2-2 had increased susceptibility to imidacloprid and fipronil, representing a possible trade-off with virulence. In contrast, a population with virulence to the highly resistant variety PTB33 was 4.88 × more resistant to imidacloprid and 3.18 × more resistant to BPMC compared to planthoppers of the same origin but reared on the susceptible variety IR22. Our results suggest complex relations between insecticide resistance and virulence that vary according to insecticidal toxins and resistance genes, and include potentially increased insecticide-susceptibility (a trade-off) as well as common detoxification mechanisms (a benefit).

Elevated temperatures diminish the effects of a highly resistant rice variety on the brown planthopper

“…PTB33 possesses at least two genes for resistance to the planthopper ( BPH32 and BPH26 [synonym with BPH2 ] 20 ). IR62 is a promising source of resistance for future rice breeding because it appears counter-selective for virulence against BPH1 and BPH2 22 . We used the variety IR22 as a susceptible control in our experiments.…”

“…The BPH32 gene encodes a protein with a signal peptide and SCR-domain that likely binds to planthopper glycoproteins or tissues to inhibit feeding 20 . Selection studies have further shown that planthoppers adapted to feed on IR62 will gain virulence against the resistant variety Rathu Heenati 21 , 22 . Such virulence-adapted planthoppers often possess relatively high densities of yeast-like symbionts (YLS) compared to non-virulent planthoppers feeding on susceptible varieties, which may compensate for the effects of anti-feedants 21 , 23 .…”

Adaptation by the Brown Planthopper to Resistant Rice: A Test of Female-Derived Virulence and the Role of Yeast-like Symbionts

“…Furthermore, Horgan et al (2016) [ 37 ] found that ca 80% of the non-adapted nymphs that survive feeding on IR62 are females and, among these, between 20–50% can have swollen abdomens—indicating potentially high reproductive output [ 37 ]. Nevertheless, egg laying and population build-up are often severely inhibited on IR62, even where planthoppers appear otherwise adapted to feed and grow on the variety—as seen in this study ( Table 1 ) and indicated in a further selection study using the same IR62-planthopper system [ 39 ]. These observations suggest that virulence adaptation results from a combination of adapted traits working on different aspects of the planthopper’s complete life cycle.…”

“…Our planthoppers also demonstrated partial adaptation to IR62 (they survived and developed well but were inefficient feeders and had slow population growth). Partial virulence may be of little benefit to planthoppers and leafhoppers that cannot build up populations in the field because of poor egg-laying capacity on a resistant host—as demonstrated in this and other studies [ 39 ]. However, even partial resistance seems to be stable in populations that are returned for several generations to a susceptible host [ 9 , 46 , 47 ].…”

“…Associated with selection for virulence in IR62, we noted that the survival of nymphs from the selected populations was marginally lower than in avirulent populations and male longevity was also lower—indicating possible trade-offs with virulence. In a related study, Horgan et al (2020) [ 39 ] found that IR62-selected planthoppers were capable of feeding on a range of varieties with other resistance genes and were less selective of rice varieties (whether resistant or susceptible) in general; furthermore, the selected planthoppers often had relatively high resistance to Fipronil but low resistance to Imidacloprid and BPMC. Such trade-offs may underlie the durability of IR62 and its resistance genes ( BPH3 and BPH32 ).…”