Adaptation of Musca domestica L. Field Population to Laboratory Breeding Causes Transcriptional Alterations

Dorte H Højland,Karl-Martin Vagn Jensen,Michael Kristensen,John Vontas

doi:10.1371/journal.pone.0085965

Abstract

BackgroundThe housefly, Musca domestica, has developed resistance to most insecticides applied for its control. Expression of genes coding for detoxification enzymes play a role in the response of the housefly when encountered by a xenobiotic. The highest level of constitutive gene expression of nine P450 genes was previously found in a newly-collected susceptible field population in comparison to three insecticide-resistant laboratory strains and a laboratory reference strain.ResultsWe compared gene expression of five P450s by qPCR as well as global gene expression by RNAseq in the newly-acquired field population (845b) in generation F1, F13 and F29 to test how gene expression changes following laboratory adaption. Four (CYP6A1, CYP6A36, CYP6D3, CYP6G4) of five investigated P450 genes adapted to breeding by decreasing expression. CYP6D1 showed higher female expression in F29 than in F1. For males, about half of the genes accessed in the global gene expression were up-regulated in F13 and F29 in comparison with the F1 population. In females, 60% of the genes were up-regulated in F13 in comparison with F1, while 33% were up-regulated in F29. Forty potential P450 genes were identified. In most cases, P450 gene expression was decreased in F13 flies in comparison with F1. Gene expression then increased from F13 to F29 in males and decreased further in females.ConclusionThe global gene expression changes massively during adaptation to laboratory breeding. In general, global expression decreased as a result of laboratory adaption in males, while female expression was not unidirectional. Expression of P450 genes was in general down-regulated as a result of laboratory adaption. Expression of hexamerin, coding for a storage protein was increased, while gene expression of genes coding for amylases decreased. This suggests a major impact of the surrounding environment on gene response to xenobiotics and genetic composition of housefly strains.

Highlights

The housefly (Musca domestica L.) is a highly mobile cosmopolitan pest, which comes into contact with excreta, carcasses, garbage and other septic matter, and is intimately associated with humans, our food and utensils
For the efficacy evaluation of insecticides, including resistance risk assessments, bioassays are pivotal. In this context bioassays are performed with an insecticide-susceptible reference laboratory strain and usually a series of resistant laboratory populations as well as field populations [5,6]
Transcriptome analysis has become a valuable alternative to the more time-consuming qPCR, but it is still limited by the extensive bioinformatics skills required by the biologist for proper data analysis [14]

Summary

Introduction

The housefly (Musca domestica L.) is a highly mobile cosmopolitan pest, which comes into contact with excreta, carcasses, garbage and other septic matter, and is intimately associated with humans, our food and utensils. For the efficacy evaluation of insecticides, including resistance risk assessments, bioassays are pivotal In this context bioassays are performed with an insecticide-susceptible reference laboratory strain and usually a series of resistant laboratory populations as well as field populations [5,6]. It is only the heterogeneous nature of field populations that allows for the selection of rare variants corresponding to resistance alleles which are likely to trigger control failure [7]. The highest level of constitutive gene expression of nine P450 genes was previously found in a newly-collected susceptible field population in comparison to three insecticide-resistant laboratory strains and a laboratory reference strain

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Conclusion