Odor, Not Performance, Dictates Bemisia tabaci's Selection between Healthy and Virus Infected Plants.

Gong Chen,Baoyun Xu,Huixin Zheng,Qingjun Wu,Wen Xie,Qi Su,Xin Liu,Shaoli Wang,Xuguo Zhou,Xiaobin Shi,Zhengke Peng,Youjun Zhang

doi:10.3389/fphys.2017.00146

Abstract

Although, insect herbivores are generally thought to select hosts that favor the fitness of their progeny, this “mother-knows-best” hypothesis may be challenged by the presence of a plant virus. Our previous study showed that the whitefly, Bemisia tabaci, the obligate vector for transmitting Tomato yellow leaf curl virus (TYLCV), preferred to settle and oviposit on TYLCV-infected rather than healthy host plant, Datura stramonium. The performances of B. tabaci larvae and adults were indeed improved on virus-infected D. stramonium, which is consistent with “mother-knows-best” hypothesis. In this study, B. tabaci Q displayed the same preference to settle and oviposit on Tomato spotted wilt virus (TSWV)-infected host plants, D. stramonium and Capsicum annuum, respectively. As a non-vector of TSWV, however, insect performance was impaired since adult body size, longevity, survival, and fecundity were reduced in TSWV infected D. stramonium. This appears to be an odor-mediated behavior, as plant volatile profiles are modified by viral infection. Infected plants have reduced quantities of o-xylene and α-pinene, and increased levels of phenol and 2-ethyl-1-hexanol in their headspace. Subsequent behavior experiments showed that o-xylene and α-pinene are repellant, while phenol and 2-ethyl-1-hexanol are attractive. This indicates that the preference of B. tabaci for virus-infected plants is modulated by the dynamic changes in the volatile profiles rather than the subsequent performances on virus-infected plants.

Highlights

IntroductionResource allocation by heterotrophs has been studied extensively, the extent to which their behavioral responses is manipulated by pathogens/parasites reflects the fine-tuned evolutionary adaptation in nature (Roy and Raguso, 1997; Ebbert and Nault, 2001; Eigenbrode et al, 2002; Hurd, 2003; Maris et al, 2004; Belliure et al, 2005; Lacroix et al, 2005; Lefèvre et al, 2006; Mauck et al, 2010; Bosque-Pérez and Eigenbrode, 2011)
We found that Tomato spotted wilt virus (TSWV) infection of D. stramonium increased the settling and oviposition of the non-vector B. tabaci Q on D. stramonium even though some of its life history traits were reduced
Our results demonstrated that four volatiles released from Tomato yellow leaf curl virus (TYLCV)-infected and TSWV-infected plants (o-xylene, α-pinene, phenol, and 2-ethyl-1-hexanol) can repel or attract B. tabaci Q in ways that are consistent with the effects of virus infection on host behavior (Figures 4, 5)

Summary

Introduction

Resource allocation by heterotrophs has been studied extensively, the extent to which their behavioral responses is manipulated by pathogens/parasites reflects the fine-tuned evolutionary adaptation in nature (Roy and Raguso, 1997; Ebbert and Nault, 2001; Eigenbrode et al, 2002; Hurd, 2003; Maris et al, 2004; Belliure et al, 2005; Lacroix et al, 2005; Lefèvre et al, 2006; Mauck et al, 2010; Bosque-Pérez and Eigenbrode, 2011). Other studies showed that mothers could make poor oviposition decisions, leading to a weak preference–performance relationship between female adults and offsprings (Rausher, 1979; Scheirs et al, 2004; Digweed, 2006; Gripenberg et al, 2007). These “bad motherhood” cases have caused extensive debates (Mayhew, 2001; Gripenberg et al, 2010). Alternative hypotheses include optimal foraging (Scheirs et al, 2000), enemy-free space (Denno et al, 1990), and insect neural capacity (Bernays, 2001)

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Results

Conclusion