Phosphine Resistance in the Rust Red Flour Beetle, Tribolium castaneum (Coleoptera: Tenebrionidae): Inheritance, Gene Interactions and Fitness Costs

Abstract

The recent emergence of heritable high level resistance to phosphine in stored grain pests is a serious concern among major grain growing countries around the world. Here we describe the genetics of phosphine resistance in the rust red flour beetle Tribolium castaneum (Herbst), a pest of stored grain as well as a genetic model organism. We investigated three field collected strains of T. castaneum viz., susceptible (QTC4), weakly resistant (QTC1012) and strongly resistant (QTC931) to phosphine. The dose-mortality responses of their test- and inter-cross progeny revealed that most resistance was conferred by a single major resistance gene in the weakly (3.2×) resistant strain. This gene was also found in the strongly resistant (431×) strain, together with a second major resistance gene and additional minor factors. The second major gene by itself confers only 12–20× resistance, suggesting that a strong synergistic epistatic interaction between the genes is responsible for the high level of resistance (431×) observed in the strongly resistant strain. Phosphine resistance is not sex linked and is inherited as an incompletely recessive, autosomal trait. The analysis of the phenotypic fitness response of a population derived from a single pair inter-strain cross between the susceptible and strongly resistant strains indicated the changes in the level of response in the strong resistance phenotype; however this effect was not consistent and apparently masked by the genetic background of the weakly resistant strain. The results from this work will inform phosphine resistance management strategies and provide a basis for the identification of the resistance genes.

Prevalence and potential fitness cost of weak phosphine resistance in Tribolium castaneum (Herbst) in eastern Australia

“…Pupae were removed from rearing medium and placed individually into 30-ml plastic souffle cups with 10 g of rearing medium after sexing according to the method of Hinton (1942). After adult emergence single pairs of virgin adults were placed into rearing medium (10 g) for 7 days after which the pairs were removed and the cups stored until the adult progeny emerged.…”

“…Champ and Dyte, 1976;Price and Mills, 1988;Herron, 1990;White and Lambkin, 1990;Rajendran, 1994;Benhalima et al, 2004;Pimentel et al, 2007;Opit et al, 2012). Studies on the inheritance of phosphine resistance in T. castaneum show that there are two broad levels of resistance (weak and strong) in this species, with two major genes (rph1 and rph2) controlling their expression (Bengston et al, 1999;Jagadeesan et al, 2012). Insects with weak resistance are homozygous for rph1 and insects with strong resistance are homozygous for both rph1 and rph2.…”

“…These genes are incompletely recessive and not sex-linked. Weakly resistant strains have been reported to be up to 12.7 times more resistant than susceptible strains, and a strongly resistant strain over 431 times more resistant, based on adult mortality after a 20-h exposure to phosphine (Bengston et al, 1999;Jagadeesan et al, 2012).…”

“…Therefore, knowing if there are fitness costs associated with phosphine resistance could help in resistance management. Fitness has been investigated in a range of insect pests of stored grain using different experimental approaches (Pimentel et al, 2007;Schlipalius et al, 2008;Sousa et al, 2009;Pimentel et al, 2011;Jagadeesan et al, 2012Jagadeesan et al, , 2013Daglish et al, 2014). Some studies have used the population cage approach in which susceptible and resistant strains are hybridized and the resulting populations are reared in the absence of phosphine selection.…”

“…As mentioned earlier, there are two broad levels of resistance (weak and strong) controlled by two major genes, so it is desirable to understand fitness consequences of being weakly or strongly resistant to phosphine. Recently, Jagadeesan et al (2012) reported that there was no evidence of fitness costs associated with either weak or strong resistance in T. castaneum, using the population cage approach and phenotype testing. The study used a single segregating population each from the following crosses: susceptible  weakly resistant, weakly  strongly resistant cross and susceptible  strongly resistant.…”