Relative contribution of genetic and environmental factors to determination of wing morphs of the brown planthopper Nilaparvata lugens

Abstract

Wing dimorphism is a fascinating feature of the ability of insects to adapt to environments. The brown planthopper (BPH) Nilaparvata lugens, a serious pest of rice, can switch between the long-and short-winged morphs. It has been known that environmental factors can affect the wing morph of BPH. However, it is still unclear whether the effect of environment is dependent on BPH genetic backgrounds or not. In the present study, we established the pure-bred lineages of short-and long-winged BPHs via multigenerational selection, and we found that survival and fecundity were similar between these 2 lineages. Wing morphs of the pure-bred lineages were almost fully dependent on genetics, but independent of the environmental factors, nymphal density and rice plant stage, 2 key factors affecting BPH wing morphs. In the unselected BPH population, short-and longwinged morphs were produced depending on those 2 environmental factors, indicating the contribution of environment to wing morph. In the wing-selected lineages, 4 developmental regulated genes of wing, NlInR1, NlInR2, NlAkt, and NlFoxo were expressed stably in the short-winged adults, but almost silenced in the long-winged adults. However, all these genes were expressed normally with a similar level in both the short-and long-winged adults in an unselected population except NlFoxo. The pure-bred lineages of long-and short-winged morphs exhibited different expression patterns of wing development-regulated genes, suggesting the genetic determination of wing morphs. Effects of environmental factors on wing morphs occurred only in the genetic mix population.

Threshold‐dependent gene regulation and partial assortative mating determine wing dimorphism of an insect

“…So, all these short‐winged morphs used in this study were the offspring of immigrated long‐winged morphs. A previous study also found that the pure‐bred lineage of the short‐winged morph of brown planthoppers was easier attained by artificial selection than that of the long‐winged morph (Zhang et al 2023). In this study, we found that the fecundity of the short‐winged strain increased as selection generation was increased, and the long‐winged strain did not change.…”

“…The full-winged and vestigial-winged ecotypes of Zelandoperla fenestrata exhibited obvious assortative mating, and almost all vestigial-winged males attempted to mate with the vestigial-winged females and no full-winged males attempted to mate with the vestigial-winged females, which facilitates rapid ecological speciation of vestigial and full-winged ecotypes (Kroos et al 2021). Assortative mating between long-and short-winged adults is not obvious or does not exist in the wild populations of the rice planthopper (Oh 1979, Peng et al 2012, Zhang et al 2023), but in this study, we found when populations were purified in wing morph, the trend towards assortative mating occurred in the short-winged strain. The short-winged males copulated with short-winged females more successfully than that with the long-winged females.…”

“…cDNA was synthetized and stored at −20°C for qPCR. SYBR Green staining method was used for qPCR, and 18s rRNA and β‐actin were selected as internal reference genes (Zhang and Liu 2020, Zhang et al 2023). qPCR reaction was performed using SYBR Premix Ex TaqTM Perfect Real Time kit (Takara, Dalian, China) in a thermocycler ABI 7500 (Applied Biosystems).…”

Range Expansion and Invasive Capacity of the Wing Di- and Polymorphic Insects: A Short Review

“…However, this polyphenism has a rather complex genetic background. The different genotypes co-existing in both N. lugens and S. furcifera are not equally sensitive to the above mentioned environmental cues (MATSAMURA, 1996;IWANAGA et al, 1986;ZHANG et al, 2022). As most genetic studies have been carried out in Japan and China, where the populations are consisted of a mixture of immigrants from different southern source populations (IWANAGA et al, 1986), it is still not clear how much relevant genetic variation exist within and between the self-sustaining tropical and subtropical populations.…”

“…This knowledge is at the moment still very scarce, and available only in a few selected "model" species: like the pea and aphid cotton aphids (Acyrthosiphon pisum Harris 1776, Aphis gossypii Glover 1877) and the rice planthoppers Nilaparvata lugens and Sogatella furcifera. However, exponential growth is expectable also in this area of research, and a synthesis of all aspects of wing polymorphism will be possible then (OGAWA et al, 2012;OGAWA and MIURA, 2014;YU et al, 2014;JI et al, 2021;ZHANG et al, 2022;). Some of the wing dimorphic and polymorphic insects are serious agricultural pests, like many species of aphids and planthoppers on many different crops, or the oriental chinch bug (Cavelerius saccharivorus Okajima, 1922) on sugarcane (FUJISAKI, 1989).…”