Inheritance and relative dominance, expressed as toxicity response and delayed development, of phosphine resistance in immature stages of Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae)

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Abstract

Fumigation of stored grain with phosphine (PH3) is used widely to control the lesser grain borer Rhyzopertha dominica. However, development of high level resistance to phosphine in this species threatens control. Effective resistance management relies on knowledge of the expression of resistance in relation to dosage at all life stages. Therefore, we determined the mode of inheritance of phosphine resistance and strength of the resistance phenotype at each developmental stage. We achieved this by comparing mortality and developmental delay between a strongly resistant strain (R-strain), a susceptible strain (S-strain) and their F1 progenies. Resistance was a maternally inherited, semi-dominant trait in the egg stage but was inherited as an autosomal, incompletely recessive trait in larvae and pupae. The rank order of developmental tolerance in both the sensitive and resistant strains was eggs > pupae > larvae. Comparison of published values for the response of adult R. dominica relative to our results from immature stages reveals that the adult stage of the S-strain is more sensitive to phosphine than are larvae. This situation is reversed in the R-strain as the adult stage is much more resistant to phosphine than even the most tolerant immature stage. Phosphine resistance factors at LC50 were eggs 400×, larvae 87× and pupae 181× with respect to reference susceptible strain (S-strain) adults indicating that tolerance conferred by a particular immature stage neither strongly nor reliably interacts with the genetic resistance element. Developmental delay relative to unfumigated control insects was observed in 93% of resistant pupae, 86% of resistant larvae and 41% of resistant eggs. Increased delay in development and the toxicity response to phosphine exposure were both incompletely recessive. We show that resistance to phosphine has pleiotropic effects and that the expression of these effects varies with genotype and throughout the life history of the insect.

Highlights

► The dominance of phosphine resistance was studied in developmental stages of R. dominica. ► Toxicity response was incompletely recessive and there was a maternally inherited factor in eggs. ► Phosphine resistance factors for life stages of differing genotypes were determined. ► Delays in development caused by phosphine exposure were determined.

Introduction

The lesser grain borer, Rhyzopertha dominica (F.), is a highly destructive coleopteran pest of stored grains worldwide. Fumigation with phosphine is the preferred control method, but extensive use of this treatment for almost half a century has led to the development of resistance in insect populations in many parts of the world (Acda et al., 2000; Collins, 1998; Lorini et al., 2007; Rajendran, 1992; Ren et al., 1994; Tyler et al., 1983). As there are few if any cost-effective alternatives to phosphine, effective management of phosphine resistance is essential for the continued protection of stored grain and other commodities.

Management of resistance requires an understanding of the evolutionary processes involved. One of the most important of these is the differential impact of insecticide dosage (selection) on the expression of resistant and susceptible genotypes, also known as relative dominance (Roush and McKenzie, 1987), as this is a strong determinant of the rate of resistance development. The relative dominance of the resistant heterozygotes is particularly important as the greater the dominance of these genotypes under treated conditions the faster resistance evolves (Onstad and Guse, 2008). In the case of phosphine, the selective agent is applied to all life stages of the insect simultaneously as commodities infested with lesser grain borer are likely to contain eggs, larvae and pupae as well as adults. Thus it is important that the expression of dominance in phosphine resistance is understood in all life stages in this species. Levels of dominance in relation to toxicity have been determined in adults of R. dominica (Bengston et al., 1999; Collins et al., 2002; Daglish, 2004; Li et al., 1994) but there is little information on its expression in immature stages of any species other than a few reports that eggs and pupal stages are generally more tolerant to phosphine than adults and larvae (Bell, 1976; Bell et al., 1977; Hole et al., 1976; Price and Mills, 1988).

Exposure to phosphine has been observed to delay the development of immature stages in two species (Nayak et al., 2003; Rajendran, 2000; Rajendran et al., 2001) but not others (Pike, 1994; Price and Bell, 1981). This phenomenon has been observed in both resistant and susceptible strains (Nayak et al., 2003) but was stronger in resistant insects. Both Nayak et al. (2003) and Rajendran (2000) observed that delayed immature development contributed to the survival of resistant insects under fumigation. Thus it may be that delay in development is a pleiotropic expression of the resistance genotype.

The objectives of the present study were to determine the mode of inheritance of phosphine resistance in the immature stages of R. dominica. We also observed physiological effects of phosphine exposure as a delay in immature development time.

Section snippets

Materials and methods

Inheritance of resistance and its expression in relation to toxicity response and immature development were observed in the immature stages of a strong resistant strain of R. dominica (QRD569) (called ‘R-strain’ in this report), a susceptible strain (QRD14) (called ‘S-strain’ in this report) and their reciprocal F1 progeny.

Toxicity – eggs

Compared with the S-strain, R-strain eggs were 37× more tolerant to phosphine at the LC50 (Table 1). This resistance factor contrasts with the 400× resistance factor estimated with respect to S-strain adults, which have a much lower tolerance to phosphine (LC50 0.00174 mg/L) (Collins et al., 2002). The response curve of the F1 (R × S) progeny in which the maternal parent was resistant, was intermediate between those of the R-strain and S-strain. The degree of dominance of −0.14 (−1 = completely

Discussion

The aim of this study was to determine the mode of inheritance of phosphine resistance in the immature stages of R. dominica as well as to quantify the relative dominance of resistance genes. To do this we exposed insects to phosphine at various developmental stages and then determined mortality as well as extension of the time required to reach adulthood.

Our results demonstrate that resistance in the egg stage is expressed as a maternally inherited semi-dominant factor. This effect was

Acknowledgements

This work was supported by the Australian Government's Cooperative Research Centre for National Plant Biosecurity and a University of Queensland International Postgraduate Research Scholarship (Awarded to RK). We thank Hervoika Pavic and Linda Bond for technical assistance and for maintaining beetle cultures.

References (39)

  • S. Rajendran

    Inhibition of hatching of Tribolium castaneum by phosphine

    Journal of Stored Products Research

    (2000)
  • R.G. Winks et al.

    The relationship between concentration and time in the toxicity of phosphine to adults of a resistant strain of Tribolium castaneum (Herbst)

    Journal of Stored Products Research

    (1986)
  • M.A. Acda et al.

    Response to phosphine of susceptible and resistant strains of Rhyzopertha dominica (Fabricius) (Coleoptera: Bostrichidae) from the Philippines

    Asia Life Sciences

    (2000)
  • P.S. Barker

    Susceptibility of eggs and young adults of Cryptolestes ferrugineus and C. turcicus to hydrogen phosphide

    Journal of Economic Entomology

    (1969)
  • M. Bengston et al.

    Inheritance of phosphine resistance in Tribolium castaneum (Caleoptera: Tenebrionidae)

    Journal of Economic Entomology

    (1999)
  • P.J. Collins

    Resistance to grain protectants and fumigants in insect pests of stored products in Australia

  • P.J. Collins et al.

    Genetics of resistance to phosphine in Rhyzopertha dominica (Coleoptera: Bostrichidae)

    Journal of Economic Entomology

    (2002)
  • P.J. Collins et al.

    Does underdosing select for resistance to phosphine?

  • G.J. Daglish

    Effect of exposure period on degree of dominance of phosphine resistance in adults of Rhyzopertha dominica (Coleoptera: Bostrichidae) and Sitophilus oryzae (Coleoptera: Curculionidae)

    Pest Management Science

    (2004)
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